Ecological Indicators 41 (2014) 1–14

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

The impact of nuclear accidents on provisioning ecosystem services
Fabienne Gralla a,d,∗ , David J. Abson b , Anders P. Møller c , Daniel J. Lang d ,Henrik von Wehrden a,eaCentre of Methods, Leuphana University Lueneburg, Scharnhorststr. 1, 21335 Lueneburg, Germany
FuturES Research Center, Leuphana University Lueneburg, Scharnhorststr. 1, 21335 Lueneburg, Germany
Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, F-91405 Orsay Cedex, FrancedInstitute of Transdisciplinarity and Ethics, Leuphana University Lueneburg, Scharnhorststr. 1, 21335 Lueneburg, GermanyeInstitute of Ecology, Leuphana University Lueneburg, Scharnhorststr. 1, 21335 Lueneburg, Germanybca r t i c l e

i n f oArticle history:
Received 8 July 2013
Received in revised form
26 November 2013
Accepted 20 January 2014
Keywords:
Caesium 137
Chernobyl
Ecosystem services
Fukushima
Nuclear accident

a b s t r a c t
Nuclear accidents lead to widespread radioactive contamination of ecosystems and related ecosystemservices, with potentially serious consequences for human well-being. Based on an initial exploratory
analysis of peer-reviewed articles related to Chernobyl and Fukushima, we identiﬁed papers whichmeasured increased Cs-137 levels in provisioning ecosystem services. We used a standardized reviewprotocol to assess (1) whether peer-reviewed science provides sufﬁcient data density and spatial coverage
to provide a coherent and comprehensive map of the global impacts of nuclear accidents on provisioning of ecosystem services; (2) whether such impacts are reported in a standardized and reproducible
way; and (3) how different safety thresholds affect the availability of food and fodder for human consumption. Based on an initial analysis of approximately 3000 articles, we identiﬁed 121 publications thatmeasured Caesium-137 levels in food, fodder and wood. We found that the comprehensive mapping of
the impacts of nuclear accidents on provisioning ecosystem services requires a considerable increase inpeer-reviewed assessments, including assessment of existing grey literature. Assessments should follow
a coherent protocol, providing consistent information on sampling location and the identiﬁcation of provisioning ecosystem services. There should be a critical dialogue on maximum allowable radiation levels
in provisioning ecosystem services and the impacts of such safe appropriation thresholds on humanwell-being.
© 2014 Elsevier Ltd. All rights reserved.

1. Introduction
Nuclear power plants are primary energy sources for 30 nations(IAEA, 2013). It has been suggested that 45 countries are actively
considering embarking upon nuclear energy programmes (World
Nuclear Association, 2014). Nuclear power is often described asa more sustainable energy solution than fossil fuels (Sokolov
and Beatty, 2009) due to the lower direct emissions of greenhouse gases (IAEA, 2012). However, the potential environmental
damage from nuclear power generation is not limited to theirnormal operations, but also the long-term direct and indirect
effects of nuclear accidents (Dangerman and Schellnhuber, 2013;
Macfarlane, 2011). Although nuclear accidents are low-frequency
events, they can cause long term impacts on a broad spatial scale∗ Corresponding author at: Centre of Methods, Leuphana University Lueneburg,
Scharnhorststr. 1, 21335 Lueneburg, Germany. Tel.: +49 4131 677 1438.
E-mail address: fabienne.gralla@leuphana.de (F. Gralla).
http://dx.doi.org/10.1016/j.ecolind.2014.01.027
1470-160X/© 2014 Elsevier Ltd. All rights reserved.

that have to be considered in the cost–beneﬁts analysis for nuclear
energy use. Therefore, assessments of the “sustainability” of nuclear
energy must also consider the full impacts of its generation, critically, including the environmental and socio-economic impacts ofnuclear accidents on the environment.
There have been two major nuclear accidents: Chernobyl(Ukraine, 1986) and Fukushima (Japan, 2011) which released Caesium 137 isotopes into the atmosphere (Lelieveld et al., 2012). In
response to these accidents monitoring programmes have been
put in place to measure ambient atmospheric gamma radiation,for example, the European Radiological Data Exchange Platform(EURDEP) with approximately 3900 monitoring stations in 33 European countries generates hourly measurements (Vries et al., 2005).
While such monitoring indicates where potential problems mightoccur, they do not provide meaningful data regarding the environmental and socio-economic impacts of nuclear accidents. There
has been considerable research carried out to evaluate the direct
impact of nuclear accidents on human health (e.g. Hoeve andJacobson, 2012; Baverstock and Williams, 2006; Ilyin et al., 1990),

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F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

but less focus on the indirect impacts on human well-being mediated through changes to ecosystems.
Long-term ecological studies are important for understanding and quantifying the effects of radiation in ecosystems acrossgenerations (Garnier-Laplace et al., 2011). Several studies haveinvestigated how radioactive substances affect migration anduptake in food chains and ecosystems (e.g. Beresford et al., 2012;
Møller and Mousseau, 2007), but ecological impact assessment
studies are limited (Møller and Mousseau, 2006, 2013) and a clear
and integrated research agenda on the impacts of nuclear accident
on ecosystems from ecological processes through to human appropriation of ecosystem functions has yet to be developed (Wehrden
et al., 2012). In particular the long-term impacts on ecosystem services are unknown.
Increased radioactivity within ecosystems following nuclear
accidents potentially reduces the availability of those ecosystems to provide ecosystem goods and services that contribute tohuman well-being. National and international regulations havebeen implemented to set the maximum permissible levels ofradioactivity in food and fodder. Adherence to such legally binding
regulations—intended to minimize harm to human health—reduces
the ability of humans to use these ecosystem services to increase
their well-being.
The Millennium Ecosystem Assessment categorizes services
provided by ecosystems into four different types: supporting, regulating, cultural and provisioning services (MEA, 2005). Following
nuclear accidents, supporting ecosystem services such as nutrient
cycling may be affected by the occurrence of long-lived and persistent nuclides such as Cs-137 through the disruption of ecosystem
functions. Regulating ecosystem services such as ﬂood protection
from wetlands (Froehlich and Wallich, 1994) may be affected, forinstance, by remediation measures to limit radioactive contamination (Davydchuk, 1997). Cultural ecosystem services impacted
by nuclear accidents are often associated with cultural practices
related to provisioning ecosystem services such as mushroom
gathering (Druzhinina and Palma-Oliveira, 2004). Provisioning
ecosystem services—the goods obtained by the ecosystems, forinstance food, fresh-water, wood, ﬁbre and fuel (MEA, 2005)—arethe most directly affected ecosystem services types from nuclear
accidents. It has been suggested that provisioning ecosystem services strongly determine human-well-being (Raudsepp-Hearne
et al., 2010). It is therefore vital that we can quantify the effectsof such thresholds on the availability of provisioning ecosystemservices after nuclear accidents.
The composition and interrelations of factors inﬂuencing Cs-137
accumulation in ecosystems are site speciﬁc, and complex—due
to issues such as bioaccumulation (Oleksyka et al., 2002), making
broad scale generalization of evolving impacts on ﬂora and fauna
difﬁcult (Beresford et al., 2007). As a consequence of these difﬁculties considerable data is required to accurately assess the impactsof nuclear accidents on ecosystems and their related services.
Here, we focus on assessing the known impact of nuclear
accidents on provisioning ecosystem services as identiﬁed in thepeer-reviewed literature. We acknowledge that there is a large
body of grey literature in the form of national monitoring reports
on radioactivity levels in provisioning ecosystem services (e.g.
MHLW, 2013a; EC, 2009). There are also monographs focusing
on the impacts of Chernobyl and Fukushima on food and agriculture (Nakanishi and Tanoi, 2013; Moberg, 1991). However,here we focus on peer-reviewed publications since this literature is not limited by national boundaries; provides reproduceable
results; additional contextual information regaring the dynamics,
interactions and impact of nuclear accidents; and draw conclusions regarding research gaps and shortcommings. There arepeer-reviewed studies that report radiation levels in a single provisioning ecosystem service across large spatial scales (e.g. Laviet al., 2006; Kalac, 2001; Mietelski et al., 1994), but these studies only provide a partial view of the impact of nuclear accidents
on provisioning ecosystem services. We assess the extent to which
the peer-reviewed science can be used to quantify the impacts of
Cs-137 contamination on provisioning ecosystem services, with a
speciﬁc focus on food, fodder and wood, after major nuclear accidents.
We addressed three aims: (1) whether the peer-reviewed science provides sufﬁcient data density and coverage to provide a
coherent and comprehensive map of the global impacts of nuclear
accidents on provision ecosystem services (which we refer to asa coherent impact grid); (2) whether scientiﬁc publications arereporting monitoring results in a standardized and reproducible
way; and (3) how different permissible radiation thresholds affectthe availability of food and fodder and therefore human well-being.
2. Material and methods
We conducted a quantitative and qualitative review of peerreviewed studies focusing on the sampling of radioactivity in food,
fodder and wood after nuclear accidents. First we identiﬁed all
publications (“full papers” in English and German) via the Scopus database (April 2012) with two search strings (see Appendix
A) including “Chernobyl” (all papers since 1986) and “Fukushima”(all papers since 2011). This search returned approximately 3300
papers. A second search on “Fukushima” to include recent papers
was conducted in November 2012 returning 76 studies.
2.1. Selection process of peer-reviewed papers
We limited the analysis to studies that measured caesium137 radioactivity (subsequently Cs-137) as the highest radiationdose to the human population after the Chernobyl and Fukushima
nuclear accidents was caused by Cs-137 deposition (Tracy et al.,2013). Moreover, Cs-137 has a half-life of 30 years, allowing
long-term impacts of radioactive accumulation on provisioning
ecosystem services to be analyzed. We considered only Becquerels(Bq) measurements, because this measure is used to set maximum permissible levels (thresholds) of radioactivity of goods thatcan be sold. One Bq describes the activity of radionuclides inwhich one nucleus decays per second on average (Kalac, 2001).
We acknowledge that provisioning ecosystem services can be
negatively affected by genetic changes as a result of radioactive accumulation in plants (Kuchma et al., 2011; Kovalchuk
et al., 2003) and animals (Røed and Jacobsen, 1995). Nevertheless, these impacts were not included in our analyses because more
knowledge is needed to understand the evolving consequences ofmutations (Kuchma et al., 2011) on provisioning ecosystem services.
We had institutional access to 1873 of the 2050 studies dealing explicitly with monitoring results and measurements on
ecosystem services. We only included papers in the analysis (Chernobyl (n = 118) and Fukushima (n = 3)) that reported actual Cs-137
radioactivity levels—illustrated or mentioned in the text, tables orgraphically—exceeding those set by the Japanese authorities after
Fukushima for food (MHLW, 2013b) and fodder (IRSN, 2012), as
we deemed this to be the lower bound threshold below which theprovision of the associated service would not be effected (Table 1).
Since no thresholds have been set for wood, we applied the recommendation of 750 Bq/kg for stemwood from the National Ukrainian
wood utilization (Davydchuk, 1999) and 100 Bq/kg for other wood
samples (bark, twigs, shoots), as assumed by Hubbard et al. (2002)
for fuel-wood. Here we should note that we did not limit the analysis to those studies that explicitly referred to the consumption of
the ﬂora and fauna under study. Therefore, this analysis relates toF. Gralla et al. / Ecological Indicators 41 (2014) 1–14

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Table 1Comparison of maximum allowed radioactivity levels in provisioning ecosystem services set in the EU and Japan.
Provisioning services in peer-reviewed articles
above current Japanese thresholds

Thresholds for Cs-137 fresh weights in Bq/kg and Bq/l

EU*

Japan (till April 2012)**

Japan (current level)***Meat, ﬁsh, mushrooms, berries, other food(vegetable, honey, lentil, rice grain, nuts)
Milk, cheese, cream, milk powder

General food1250
Milk and dairy products
1000

General foods
100
Milk
50

Baby food

Infant food
400
Water/liquid foodstuff
1000
Fodder (depending on livestock)
1250–5000
Minor foodstuff
ten times those of general food
Recommendations in some countries
for wood samples

Meat, eggs, ﬁsh, grains, vegetables
500
Drinking water, milk and dairy
products
200
n.a.

Tea (leaves)
Fodder (incl. crops)
Plants for pharmaceutical use
Non-food: wood (stemwood, fuelwood),
tobaccoDrinking water200
Feed****
500
n.a.

Infant foods
50
Drinking water
10
Feed****
500
n.a.

n.a.

n.a.

Allowed levels of total Cs 134 and Cs 137 activity in Becquerel per litre or kilogram of products which will be placed on the market (wet weight) after Chernobyl for the EU(*EEC, 1987a,b, 1989a,b, 1990) and after Fukushima for Japan (**MHLW, 2011a,b, ***MHLW 2013b, ****EC, 2011).

potential, rather than actually appropriated, provisioning ecosystem services. Only papers where the ﬂora studied was explicitly
noted as having fodder or pharmaceutical/medicinal use(s) were
included in the analysis, only edible mushroom species were considered.

all countries where studies on provisioning ecosystem services
took place. Hence the total number of scientiﬁc studies (n = 132)
and the total number of provisioning ecosystem services recorded(n = 173) is higher than the number of published peer-reviewed
papers (n = 121).

2.2. Data collection—analysis of papers(5) After which accidents did the contamination take place? (Accident)(6) and (7) Is the sampling location explicitly mentioned (Latitude/Longitude; Exactness of georeference: explicitly mentioned or inferred)?

We refrained from providing a statistical analysis due tostochastic radioactive accumulation in provisioning ecosystem services. The 121 papers analyzed showed considerable variance withregard to their spatial and temporal focus. Therefore, we undertooka mixed qualitative and quantitative analysis based on the following on nine variables extracted from each of the peer-reviewed
publications (see Appendix Table A1):
(1) Which types of provisioning ecosystem services were contaminated by Cs-137?
Ecosystem services were assigned to different provisioning
types (e.g. meat, dairy, fodder). If multiple goods of the same typewere studied at the same place only the highest radioactivity levelof one of the goods was recorded. For example, only rabbit, witha maximum level of 1360 Bq/kg, was taken from the various meatsources sampled by Fehér (1988).
(2) How high was the contamination level of the service? (Min,
Max, Mean in Becquerel)
We analyzed all provisioning ecosystem service types above
permissible thresholds (see Appendix Table A1). Where radioactivity levels were only shown over time graphically (e.g. Kostiainen,
2007; Smith et al., 2000), the highest level was estimated visuallyfrom the graph.
(3) and (4) When and where the sample was analyzed? (Year,Country)

If a speciﬁc georeference was not mentioned we took the information that inferred the approximate site of the sample(s).
(8) Was the sample measured in dry or fresh weight? (Weights)
Radioactive measurements can been reported in dry weights(Appendix Table A2), whereas maximum allowed thresholds forfood refer to fresh/wet weights (EEC, 2000). Following Kalac (2001)
all dry weight becquerel measurements of food samples can bescaled by a factor of 0.1 to estimate fresh weight contamination.
Thus, we recalculated the dry weight contamination of mushorrms
according to that approach.
(9) How long was the sampling process? (Time scale)Since radiation impacts differ in time reliable temporal data isrequired. Here we recorded the duration of the sampling process(up to one month; between one month and a year; more than one
year till ﬁve years; more than ﬁve years to ten years, more than ten
years).
All ﬁgures were made using the R 2.14.2 software(www.r-project.org) and ArcGIS 10.
3. Results

If the sampling process of the study was conducted over several years only the highest contamination of provisioning services
was recorded. Furthermore, if one provisioning ecosystem service
type has been analyzed at several locations in one country, weused the highest contamination level of one sampling location
within the country (e.g. Smith et al., 1993). Thus, we recorded

121 scientiﬁc papers—Chernobyl (n = 118) and Fukushima(n = 3)—were analyzed based on nine variables. Results show variations in data collection and reporting. There were no coherent
maximum permitted radiation levels implemented in affected
countries covering all provisioning ecosystem services.

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F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

Fig. 1. Distribution of published peer-reviewed articles on the radioactivity in provisioning ecosystem services. Publication year and duration of sampling process ofradioactivity in provisioning ecosystem service after Chernobyl and Fukushima.

3.1. Temporal-, spatial- and types of provisioning service
coverage in peer-reviewed science
The majority of the monitoring of radioactivity in food and fodder started in the ﬁrst years after Chernobyl (Fig. 1). A total of 66%(n = 107) of all studies (n = 173) were conducted for more than one
year (Fig. 1), but only 11% for ten years or more (n = 18). The overall
trend showed declining peer-reviewed publications over time withmost studies published in the ﬁrst ten years, with an increase in thedecennial anniversary years (Fig. 1).
Regarding the spatial coverage of the impacts we found thatpeer-reviewed research was patchily distributed in space (Fig. 2).
No coherent global or European impact grid on provisioning ecosystem services could be generated from the peer-reviewed studies.
The majority (58%) of the scientiﬁc research studies were locatedin the following six countries: Sweden (n = 18), Germany (n = 14),Austria (n = 11), Ukraine (n = 12), Norway (n = 11) and the United
Kingdom (n = 11) (Fig. 2). Only 39 of the provisioning ecosystemservice studies (Fig. 2 explicit location) gave explicit georeferences
for their locations. The majority of data (n = 134) could not be linked
to their speciﬁc spatial origin.
The focus on the impact of nuclear accidents on provisioning
ecosystem services varied considerably among different provisioning services “types”. The greatest focus was on radioactive
accumulation in mushrooms (n = 43) and meat (n = 40), followedby ﬁsh (n = 28) and dairy products (n = 17). It is unclear if this focus
was due to the relatively high radioactivity levels in mushrooms,
meat and ﬁsh (Fig. 3) compared to other provisioning ecosystemservices, or simply because other provisioning services were simply studied less. However, we note that other food and non-foodproducts, for instance berries and tobacco, have also shown highaccumulations in some samples (Fig. 4).

Fig. 2. Overview of the research activities on provisioning ecosystem services in peer-reviewed publications. Studies are included with monitoring results above Fukushima
thresholds set in April 2012 (MHLW, 2013a).

F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

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Fig. 3. Examples of long-term radioactive contamination in provisioning ecosystem services. Examples of maximum radioactivity (Bq/kg) in meat, ﬁsh and mushrooms (wetweights) based on samples taken more than ﬁfteen years after Chernobyl.

3.2. Impact of threshold schemes on the availability of food andfodderMaximum permissible radioactivity levels in food and otherproducts regulate market entry. Since there is no common threshold scheme, limits differ across the world (Table 1), inﬂuencing
the availability of provisioning ecosystem services after nuclear

accidents to different extents. Fig. 4 illustrates the effects of different thresholds for safe consumption of food and fodder on
the ability of humans to appropriate provisioning ecosystem services after nuclear accidents. If Fukushima thresholds had been
adopted after Chernobyl, a broader range of food and otherproducts would have been prohibited for human consumption(Figs. 4 and 5).

Fig. 4. Overview of radioactivity in food (highest value collected). For comparison safe consumption threshold levels set by the European Union (EU) and the Japanese
authority (J) are illustrated (horizontal grey lines). Baby food (one sample) and tea (three samples) were not illustrated. The category other food includes one sample of lentil,
spinach, hazelnut, rice bran and two samples of honey. Numbers above individual boxes are the sample sizes. One sample can be included with its minimum, maximum andmean level. Hence, the total number of data here is higher than the total number of samples in the study. Box plots show median, quartiles 25 and 75-percentiles.

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F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

Fig. 5. Overview of radioactivity levels in dairy products and milk, fodder and wood. For wood samples recommended levels have been used (Davydchuk, 1999; Hubbard
et al., 2002). Box plots show median, quartiles 25 and 75-percentiles. For comparison safe consumption threshold levels set by the European Union (EU) and the Japanese
authority (J) are illustrated (horizontal grey lines).

4. Discussion
Global peer-reviewed research on the impact of nuclear accidents on provisioning ecosystem services has been conducted in
25 countries. However, these scientiﬁc studies do not provide sufﬁcient spatial and temporal coverage to allow for a detailed andcoherent assessment of the impacts of nuclear accidents on provisioning ecosystem services. This is crucial for gaining knowledge
about relationships between nuclear accidents and their impacts
on human well-being.
4.1. Impact grid—variations in temporal, spatial and service types
coverage
A total of 121 peer-reviewed papers contained results on Cs137 radiation contamination (above relevant minimum statutory
safety thresholds) in provisioning ecosystem services. This number
seems to be rather low given that caesium was deposited over large
parts of Europe after Chernobyl. If publications after the Fukushima
accident follow a similar temporal trend as found for Chernobyl, we
could expect the highest number of studies to be conducted in 2013,
followed by a general decreasing trend with decennial anniversary peaks. This temporal sampling dynamic, in part, reﬂects thehalf-life decrease of radioactivity, however, increased accumulation levels in ﬂora and fauna are inﬂuenced by several factors andcan occur even several years after an accident (Beresford et al.,2007; Pel’gunov et al., 2006).
Although our data cannot provide deep insights into bioaccumulation pattern of different regions, it is an important issue forfurther investigations. Avery (1996) stated that direct biologicalaccumulation of Cs-137 from the environment occurs in lower
trophic levels whereas higher trophic levels might accumulate Cs137 due to ingestions of food or inhalation and absorption fromthe environment. Rowan and Rasmussen (1994) tested several
inﬂuencing factors on ﬁsh and pointed out that among other ecological factors the trophic level of the ﬁsh plays a crucial role.
Yamazaki et al. (2012) suggested that the contamination of forest soil affects ﬂora and fauna with higher accumulation rates onhigher trophic levels. To investigate bioaccumulation in forest soils,
animals and food samples long-term monitoring programmes are
required (Yamazaki et al., 2012). Thus, it is important for the scientiﬁc community to collect long-term data. Since several sites in
Europe are still affected by the fallout from Chernobyl 20 years after
the accident (Fig. 3), it is crucial to use reliable data to gain knowledge on the long-term impacts of nuclear accidents on provisioning
ecosystem services.
The spatial distribution of peer-reviewed studies was uneven.
The distance to nuclear accidents appears to play no signiﬁcantrole, so there seems to be no higher risk perception, fostering
more research, in the Ukraine for instance than in Sweden. Nor
do ofﬁcial attitudes towards nuclear power generation appear to
pay a role in research efforts. Countries phasing out nuclear power(Germany), and countries with no nuclear facilities (Austria) bothconducted research. Similarly, countries that repealed phase-out
plans (Sweden) or are still discussing the building of nuclear facilities (Norway) invested similar research efforts on the impact of
nuclear accidents on provisioning ecosystem services.
Radioactive accumulation of Cs-137 in food and other provisioning services shows a patchy distribution. For example,
accumulation levels in ﬁsh, differed among species and populations

F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

with variation among years (Hammar et al., 1991). Radioactive
accumulation differences depend on many factors such as theamount of soil ingested by animals (Beresford and Howard, 1991)
and their movement habits (Karlén et al., 1991). Game using lesscontaminated habitats has a high tendency to accumulate lower
levels of Caesium-137 in their muscles (Lowe and Horrill, 1991).
Nevertheless, contamination levels in fauna may be increasing evenwhen ambient radioactivity is decreasing (Pel’gunov et al., 2006).
This diversity of inﬂuencing factors on a regional scale hinders
appropriate generalization of results (Beresford et al., 2007). That is
one example of the high level of uncertainty regarding radioactive
accumulation in food chains that makes it more difﬁcult to model(Wright et al., 1998). Data sampling on the impacts of nuclear accidents on provisioning ecosystem services requires a higher densityof spatial, temporal and species-speciﬁc data to create a coherent
impact grid and to allow analysis of the interrelated impacts onother ecosystem services.
The small number of studies on the ecological impact of released
radioactivity may be a result of very limited funding for large scale
research attempting to determine the consequences of radiation
exposure (Møller and Mousseau, 2006) and a scarcity of independent scientists able to undertake such assessments (Møller andMousseau, 2013). While funding seemed to be available in the
short-term—the majority of studies were published within the ﬁrst
ten years after Chernobyl (Fig. 1)—long-term monitoring data after
nuclear accidents may help to understand the behaviour of radioactive material (Nihei, 2013) and the full impact of such accidents on
ecosystem services.
The peer-reviewed research was also patchy with regard to thetypes of provisioning ecosystem services studied. This patchiness inresearch effort might be inﬂuenced by existence of safe consumption threshold schemes. Since more research is conducted on foodproducts (such as meat, mushrooms, ﬁsh and milk) that are regulated than on non-food products (such as tobacco and wood) thatare not. The impacts on marine and coastal ecosystems and theirservices should be a focus of research efforts after the Fukushima
accidents, since highly radioactive water has been introduced to theocean (Buesseler et al., 2011, 2012), but it is not clear this will beinﬂuenced by the existent (or not) of safe consumption thresholds.
With a few exceptions (e.g. Merz et al. (2013) and Strand et al.
(1987)) ofﬁcial governmental radioactivity measurements of foodand fodder are rarely presented in peer-reviewed journals. One
challenge to collating Cs-137 radioactive impact data is connectedwith the fact that some studies on provisioning ecosystem services are not written in English (e.g. Pel’gunov et al., 2006; Skurdal
et al., 1987). Some communication of monitoring data does takes
place via European reports, (e.g. EC, 2009), and this is an importantﬁrst step to foster data analysis and transparent communication
efforts. However, it is still important to have open data access togovernmental monitoring results to enable peer-reviewed analysisof relationships and patterns within and between these large scale
governmental monitoring schemes. This would provide a greater
understanding of the link between radioactive contamination andits impacts on ecosystem services and the consequences for humanwell-being.
4.2. Reporting of monitoring results—improvements needed
Clear communication requires transparent and coherent reporting of analyses and results is currently hindered by a lack oftranslation of original reports into English (Fairlie and Sumner,
2006). Information about the spatial location of studies should
be included, and it would be preferable to have speciﬁc georeference data for every sampling location. If the location of study
samples is unavailable the spatial analysis of underlying patterns,
for instance the potential impacts on other related ecosystem

7

services, is hampered. It is crucial to have a spatially explicit
database of these studies since radioactivity after nuclear accidents
appears to be patchily distributed over large distances, making
appropriate impact assessment challenging. The use, or non-use,of contaminated samples recorded within studies on provisioning
ecosystem services should to be mentioned. Otherwise the impactsof nuclear accidents on ecosystem services cannot be assessed withany degree of certainty (i.e. we cannot differentiation between
potential health effects due to consumption of contaminated goods
from the economic loss due to non-consumption of contaminatedgoods).
4.3. The impact of threshold schemes on the availability of foodand fodder
Maximum permissible levels for radioactive Cs-137 contamination in food and fodder inﬂuence the availability of such goods
by regulating market entry. When products cannot be sold, livelihoods may be adversely affected. Threshold levels differ in several
countries leading to different amounts of available food (Beach,
1990; Skurdal et al., 1987). If contamination levels lead to longterm restrictions, entire farming systems can be disturbed leading
to a long-term decrease in availability (Smith et al., 2000; Kerrand Mooney, 1988). The use of contaminated food and fodder differs among countries based on national safe threshold schemes(Fig. 4). Since the behaviour of radionuclides such as Cs-137 does
not change regarding national borders, it is neither clear on what
basis these scheme should differ, nor the scientiﬁc justiﬁcation fora given threshold level.
4.3.1.1. Diversity of numbers and recommendations
Since Chernobyl the permissible radiation limits differed within
European borders. For example, Sweden established its own limits
at 300 Bq/kg for general food and raised the limit for Saami food(reindeer meat, ﬁsh and game) up to 1500 Bq/kg (Beach, 1990).
Meat intended for import into the EU was not allowed to show
higher total Caesium values than 600 Bq/kg, whereas meat for use
inside the EU could have levels up to 1250 Bq/kg (Table 1). Different levels have been established in Norway where they decided inJune 1986 to allow the selling of dairy products and infant foodunder 370 Bq/kg and others food up to 600 Bq/kg. In Sweden milk
should not exceed 300 Bq/l and in some cases even milk with Caesium levels above 40 Bq/l were not allowed to be transferred todairies (Karlén et al., 1991). Some countries proposed their own
recommendations for forest products, for example, in the Ukraine
stemwood with radioactivity above 750 Bq/kg is limited to industrial use (Davydchuk, 1999). In Sweden where large parts of thecountry is covered by forests the Swedish Radiation Safety Authority suggested no use of wood ashes from the combustion of biofuels
as fertilizer when Cs-137 exceed the 5000 Bq/kg, with 100 Bq/kg set
as the permissible level for fuelwood (Hubbard et al., 2002).
Threshold schemes vary among countries and include a selection of provisioning ecosystem services that has been widely
deﬁned as food and fodder. The European Commission has included
plants for medicinal or pharmaceutical use in threshold schemes(EEC, 1989b), while some provisioning ecosystem services are
only part of recommendations (e.g. wood). The implementation ofthresholds rely on linear effects, although as Møller and Mousseau(2013) pointed out radiation below such thresholds may still havenegative effects. Thus, an implementation of maximum allowed
radiation levels offers a level of security, but as the response toradiation differs largely among species and traits, there may still
be signiﬁcant radiation risks (Møller and Mousseau, 2013). The
negative impact on human health should be considered in conjunction with the socio-economic consequences of loss of provisionof ecosystem services. Threshold schemes to tackle the negative8

F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

impacts on human health caused by radiation rarely give anappropriate estimation on how long, where and to what extent
provisioning ecosystem services are affected, making a full impact
analysis of the impacts of nuclear accidents (and the related safe
consumption regulations) have on human well-being more challenging. To address this challenge, ﬁrst, we need reliable impact
data to assess where and how single services are affected, and,second, it is crucial to understand patterns of feedbacks andrelationships between affected ecosystem services to enable andsustain human well-being. A clear and transparent considerationof acceptable safe radiation thresholds in provisioning ecosystemservices is required. Such an assessment should include the potential trade-offs between the direct (health) and indirect (degradationof ecosystem services) effects on human well-being of these thresholds.
4.3.1.2. Linkages and feedbacks—impacts in a complex world
Knowledge about consequences of our actions often lacks anunderstanding of all the underlying patterns, feedback mechanisms and interrelations between impacts (Weinstein et al., 2013).
The total impacts on human well-being after nuclear accidents
are yet to be fully analyzed and understood. Ecosystems areaffected by increased radiation in their processes and services
on a broad scale and long-term perspective (Wehrden et al.,2012). Since these services are interlinked and inﬂuence humanwell-being, impact analysis of ecosystem services from nuclear
accidents should play an important role in fostering appropriate
decision-making regarding nuclear power. Data on the impact onprovisioning ecosystem services are rare in peer-reviewed studies, and knowledge on the interrelations between impacts on all
ecosystem services is almost non-existent. Nuclear accident impact
analysis could be improved by using existing monitoring data andincreasing research efforts in peer-reviewed studies. The impact
of increased radiation after a nuclear accident requires research
approaches analyzing affected ecosystems based on high data density of radiation measurements. It is important to use a more
holistic approach of sustainability assessment on nuclear energy byincluding all the risks to human well-being from nuclear accidents(Stamford and Azapagic, 2011). This should include information
about the potential degradation of ecosystem services due to radiation.
5. Conclusion
We conclude that scientiﬁc research conducted to assess theimpact on provisioning ecosystem services after nuclear accidents
in peer-reviewed studies might be inﬂuenced by a “don’t-askdon’t-tell” maxim. Hence, we suggest that the impacts of nuclear
accidents on provisioning ecosystem services should be puton the agenda of nuclear energy assessments. Global scientiﬁc
peer-reviewed research on this topic is currently, at best, limited

and patchy. The degree of information varies regarding sampling
location, sampling time as well as use, or non-use, of the studied plants and animals as provisioning ecosystem services. To
create a coherent grid of impacts of nuclear accidents on provisioning ecosystem services, we highlight the following aspects. First,
there is a need for increased peer-reviewed research regarding theimpact of nuclear accidents on provisioning ecosystem services.
This can be achieved by reviewing the existing national reports
and subsequent publication of the results in English. Further global
measurements of short- and long-term results should be collected
for an appropriate impact assessment in a central database. Second, research studies need to follow a coherent protocol enablingcommon information on sampling location and use of the potential
provisioning ecosystem services. Third, there should be a critical
dialogue regarding the maximum permissible radiation levels inprovisioning ecosystem services and what these rules mean forhuman well-being.
Acknowledgments
Patric Brandt and Tillman Kiehn helped structuring the initial
draft. Heike Zimmermann assisted in plotting the graphs. FG was
funded by a scholarship ﬁnanced by Leuphana University. Thanks
to the anonymous reviewers for their constructive comments.
Appendix A.
See Tables A1 and A2.
A 3 Search strings
Your query: TITLE-ABS-KEY(chernobyl) AND PUBYEAR > 1985
AND (LIMIT-TO(DOCTYPE, “ar”)) AND (LIMIT-TO(LANGUAGE,“English”) OR LIMIT-TO(LANGUAGE, “German”)) AND (LIMITTO(SUBJAREA, “ENVI”) OR LIMIT-TO(SUBJAREA, “ENER”) OR LIMITTO(SUBJAREA, “PHYS”) OR LIMIT-TO(SUBJAREA, “BIOC”) OR LIMITTO(SUBJAREA, “AGRI”) OR LIMIT-TO(SUBJAREA, “PHAR”) OR LIMITTO(SUBJAREA, “CHEM”)) AND (EXCLUDE(SUBJAREA, “MEDI”) OR
EXCLUDE(SUBJAREA, “HEAL”) OR EXCLUDE(SUBJAREA, “NEUR”) OR
EXCLUDE(SUBJAREA, “IMMU”) OR EXCLUDE(SUBJAREA, “COMP”)
OR EXCLUDE(SUBJAREA, “PSYC”) OR EXCLUDE(SUBJAREA, “MATH”)
OR EXCLUDE(SUBJAREA, “VETE”) OR EXCLUDE(SUBJAREA, “ARTS”)
OR EXCLUDE(SUBJAREA, “DECI”) OR EXCLUDE(SUBJAREA, “DENT”)
OR EXCLUDE(SUBJAREA, “NURS”))
Your query: TITLE-ABS-KEY(fukushima) AND PUBYEAR > 2010
AND (LIMIT-TO(LANGUAGE, “English”) OR LIMIT-TO(LANGUAGE,“German”))
AND(EXCLUDE(SUBJAREA,“MEDI”)OR
EXCLUDE(SUBJAREA, “COMP”) OR EXCLUDE(SUBJAREA, “ARTS”) OR
EXCLUDE(SUBJAREA, “MATH”) OR EXCLUDE(SUBJAREA, “HEAL”)
OR EXCLUDE(SUBJAREA, “NEUR”) OR EXCLUDE(SUBJAREA, “NURS”)
OR EXCLUDE(SUBJAREA, “IMMU”) OR EXCLUDE(SUBJAREA, “PSYC”)
OR EXCLUDE(SUBJAREA, “VETE”)) AND (LIMIT-TO(DOCTYPE, “ar”))

Table A1
The standardized analysis is based on nine indicators.
Different variables of interest

Content

Group of provisioning ecosystem services

Fish, meat, mushrooms, dairy products, crops, fodder, foodstuff (incl. tea, honey, vegetables, hazelnuts), berries, milk,
pharmaceutical use, wood, tobacco
e.g. Min: 12,000
e.g. 1987
Name of the country today (e.g. German Democratic Republic = Germany; Scotland, Wales, England = UK)
Chernobyl: 2, Fukushima: 3e.g. 62◦ 62 N, 17◦ 07 E
not speciﬁc (no georeference or city → georeference of capital taken): 0, inferred (city or other points have been
mentioned of which georeference could be developed): 1, explicit (georeference attached in paper): 2
No: 0, Yes: 1
Up to one month: 0, more than one month till one year: 1, more than one year till ﬁve years: 2; more than ﬁve years
till ten years: 3, more than ten years: 4

Becquerel level: Min, Max, Mean
Year
Country
Accident
Latitude/longitude
Exactness of georeferences
Dry weight
Time scale of research study

Table A2
Articles included in the analysis.
Year

Title

Group

Ahman, B., Wright, S.M., Howard, B.J.
Ajdacic, N., Martic, M.

2001
1989
1989
1989
1989
1989
1989
1996
1996
2001
2001
1998
1986
2003
2003
1999

Effect of origin of radiocaesium on the transfer from fallout to reindeer meat
Contamination of some important kinds of plants by ﬁssion-productsContamination of some important kinds of plants by ﬁssion-productsContamination of some important kinds of plants by ﬁssion-productsContamination of some important kinds of plants by ﬁssion-productsContamination of some important kinds of plants by ﬁssion-productsContamination of some important kinds of plants by ﬁssion-products
Accumulation and long term behaviour of radiocaesium in Norwegian fungi
Accumulation and long term behaviour of radiocaesium in Norwegian fungiLong-term studies on transfer of Cs-137 from soil to vegetation and to grazing lambs in a mountain area in Northern Sweden
Long-term studies on transfer of Cs-137 from soil to vegetation and to grazing lambs in a mountain area in Northern Sweden
Root uptake of Cs-137 and Sr-90 by rye-grass on various soils in the CISRadioactivity in air, rain, soil, plants and food after the chernobyl incident
Determination of radionuclides in foods from Minsk, Belarus, from Chernobyl to the present
Determination of radionuclides in foods from Minsk, Belarus, from Chernobyl to the present
Radiocaesium activity concentrations in the fruit-bodies of macrofungi in Great Britain and an assessment of dietary intake
habitsRadioactivity in mushrooms in northeast Italy following the chernobyl accident
Radioactivity in mushrooms in Northeast Italy following the chernobyl accident
Radioactive fallout from the chernobyl nuclear-reactor accident
Transfer of chernobyl fallout cesium radioisotopes in the cow food-chain

Meat
Meat
Dairy product
FodderBaby foodMeat
PharmaMushrooms
Mushrooms
Mushrooms
Meat
FodderMeat
Dairy product
Dairy product
Mushrooms

Fish
Meat

Amundsen, I., Gulden, G., Strand, P.
Andersson, I., Lonsjo, H., Rosen, K.
Askbrant, S., Sandalls, J.
Bangert, K., et al.
Baratta, E.J.
Barnett, C.L., Beresford, N.A., Self, P.L., Howard, B.J.,
Frankland, J.C., Fulker, M.J., Dodd, B.A., Marriott, J.V.R.
Battiston, G.A., Degetto, S., Gerbasi, R.,
Sbrignadello, G.
Beiriger, J.M., Failor, R.A., Marsh, K.V., Shaw, G.E.
Belli, M., Drigo, A., Menegon, S., Menin, A., Nazzi, P.,
Sansone, U., Toppano, M.
Belova, N.V., Emeland’yanova, N.G.
Beresford, N.A., Barnett, C.L., Crout, N.M.J., Morris, C.C.

1989
1989
1988
1989

Bradley, E.J., Wilkins, B.T.

1989

Bretten, S., Gaare, E., Skogland, T., Steinnes, E.
Brittain, J.E., Gjerseth, J.E.

1992
2010

Bunzl, K., Kracke, W., Vorwohl, G.
Constantinescu, B., Galeriu, D., Ivanov, E.A., Pascovici, G.,
Plostinaru, D.
Cooper, E.L., Zeiller, E.,
Ghodsesphahani, A., Makarewicz, M.,
Schelenz, R., Frindik, O., Heilgeist, M.,
Kalus, W.

1988
1988

Status of reproductive system of bony ﬁshes of Teterev River and Kiev Reservoir after 20 years of Chernobyl catastropheRadiocaesium variability within sheep ﬂocks: Relationships between the Cs-137 activity concentrations of individual ewes
within a ﬂock and between ewes and their progeny
Inﬂuence of husbandry on the transfer of radiocesium from feed to dairy product during the winter that followed thechernobyl reactor accident
Investigations of radiocesium in the natural terrestrial environment in Norway following the chernobyl accident
Long-term trends and variation in Cs-137 activity concentrations in brown trout (Salmo trutta) from Ovre Heimdalsvatn, aNorwegian subalpine lake
Transfer of chernobyl-derived cs-134, Cs-137, I-131 and Ru-103 from ﬂowers to honey and pollen
Determination Of I-131, Cs-134, Cs-137 in plants and cheese after chernobyl accident in Roumania

1992
1992
1992
1992
1992
1992
1995

Radioactivity in food and total diet samples collected in selected settlements in the USSRRadioactivity in food and total diet samples collected in selected settlements in the USSRRadioactivity in food and total diet samples collected in selected settlements in the USSRRadioactivity in food and total diet samples collected in selected settlements in the USSRRadioactivity in food and total diet samples collected in selected settlements in the USSRRadioactivity in food and total diet samples collected in selected settlements in the USSR
Evaluation of Cs-137 activity in plant drugs and in some phytoderivatives from Chernobyl accident up to present (1986–1994)

Mushrooms
Dairy productBerriesFish
Mushrooms
Fish
Pharma

1992
1992
1992
1993
2010
1993

Radioactive contamination of food sampled in the areas of the USSR affected by the chernobyl disasterRadioactive contamination of food sampled in the areas of the USSR affected by the chernobyl disasterRadioactive contamination of food sampled in the areas of the USSR affected by the chernobyl disasterRadioactive contamination of food sampled in the areas of the USSR affected by the chernobyl disasterTransfer of Radiocesium into Wild Boar Meat
Sources of variation in post-Chernobyl radiocaesium in brown trout, Salmo trutta L, and Arctic charr, Salvelinus alpinus (L),from six Cumbrian lakes (northwest England)
Sources of variation in post-chernobyl radiocesium in ﬁsh from 2 cumbrian lakes (north-west England)Mushrooms
FodderDairy product
Mushrooms
Meat
Fish

Radioactivity in mushrooms, mosses and soil samples of deﬁned biotops in sw Bavaria— 2 years after chernobyl
Natural and chernobyl-caused radioactivity in mushrooms, mosses and soil-samples of deﬁned biotops in sw Bavaria
Paddy-ﬁeld contamination with 134Cs and 137Cs due to Fukushima Dai-ichi Nuclear Power Plant accident and soil-to-ricetransfer coefﬁcients

Mushrooms
Mushrooms
Food

Curini, M., Rosati, O., Borio, R., Saetta, D.M.S., Cicioni, R.,
Forini, N., Rongoni, A., Dipilato, A.C.
Deruig, W.G., Vanderstruijs, T.D.B.

Dvorak, P., Snasel, P., Benova, K.
Elliott, J.M., Elliott, J.A,. Hilton, J.
Elliott, J.M., Hilton, J., Rigg, E., Tullett, P.A., Swift, D.J.,
Leonard, D.R.P.
Elstner, E.F., Fink, R., Holl, W., Lengfelder, E., Ziegler, H.
Elstner, E.F., Fink, R., Holl, W., Lengfelder, E., Ziegler, H.
Endo et al.

2009
1996

Mushrooms
Mushrooms
Mushrooms
Fodder

1992
1989
1987
2013

Dairy product
Meat
Fish
Food
Dairy productF. Gralla et al. / Ecological Indicators 41 (2014) 1–14

Author

Fish

9

10

Table A2 (Continued)
Author

Year

Title

Group

Feher, I.

1988
1988
1996
1996
2009
1994
1992

Experience in Hungary on the radiological consequences of the chernobyl accident
Experience in Hungary on the radiological consequences of the chernobyl accident
Radiocesium in wild animals after the reactor accident in Chernobyl
Radiocesium in wild animals after the reactor accident in Chernobyl
Seasonality of Cs-137 in roe deer from Austria and Germany
Cs-137 in ﬁsh of some lakes and rivers of the bryansk region and north-west RUSSIA in 1990–1992
Radiocesium in muscle-tissue of reindeer and pike from Northern Sweden before and after the chernobyl accident—aretrospective study on tissue samples from the Swedish-environmental-specimen-bankCs-137 transfer from forage to dairy product and its removal by clay treatment
Radionuclide monitoring in northern-Ireland of the chernobyl nuclear-reactor accident
Radionuclides and heavy metals concentrations in Turkish market tea

Meat
PharmaMushrooms
Meat
Meat
Fish
Meat

Activity of cesium-134 and cesium-137 in game and mushrooms in Poland
Activity of cesium-134 and cesium-137 in game and mushrooms in Poland
Remedial measures against radioactive cesium in Swedish lake ﬁsh after chernobyl

Mushrooms
Meat
Fish
Fish
Wood
Mushrooms
Meat
Foodstuff
BerriesDairy product
Food
Fish
FodderFodderMeat

Fielitz, U.
Fielitz, U., Klemt, E., Strebl, F., Tataruch, F., Zibold, G.,
Fleishman, D.G., Nikiforov, V.A., Saulus, A.A., Komov, V.T.
Forberg, S., Odsjo, T., Olsson, M.

1988
1987
2011

Hessen, D.O., Skurdal, J., Hegge, O., Hesthagen, T.
Higaki, T., Higaki, S., Hirota, M., Akita,K., Hasezawa, S.
Hohmann, U., Huckschlag, D.

1994
1994
1992
1999
1997
1989
1988
1988
1988
1988
1988
2002
2012
2012
2005

Horrill, A.D., Kennedy, V.H., Paterson, I.S., McGowan, G.M.

1995

Ikaheimonen, T.K., Saxen, R.
Johanson, K.J., Bergstrom, R.

Lepicard, S., Dubreuil, G.H.

2002
1989
1989
1999
1994
1994
1991
1991
1995
1990
2007
2007
2007
1996
1992
1995
2013
2013
2001

Lettner, H., Griesebner, A., Peer, T.,
Hubmer, A.K., Pintaric, M.
Lettner, H., Hubmer, A., Bossew, P.,
Strebl, F.
Lowe, V.P.W., Horrill, A.D.
Lowe, V.P.W., Horrill, A.D.

2006
2006
2007
2007
1991
1988

Jonsson, B., Forseth, T., Ugedal, O.
Kalas, J.A., Bretten, S., Byrkjedal, I., Njastad, O.
Kammerer, L., Hiersche, L., Wirth, E.
Karlen, G., Johanson, K.J., Bergstrom, R.
Karlen, G., Johanson, K.J., Bertilsson, J.
Kliment, V., Bucina, I.
Kostiainen, E.

Koulikov, A.O.
Koulikov, A.O., Ryabov, I.N.
Kritidis, P., Florou, H.
Lehto et al.

Radioactivity in straw and energy forestry used for energy production in Sweden
Natural and artiﬁcial radionuclides in selected styrian soils and plants before and after the reactor accident in chernobyl
Chernobyl—its Impact on austria
Chernobyl—its impact on Austria
Chernobyl—its impact on Austria
Chernobyl—its impact on Austria
Chernobyl—its impact on Austria
Radiocesium decay in populations of brown trout and Arctic char in the alpine Atna area, south-eastern Norway
Radionuclide Analysis on Bamboos following the Fukushima Nuclear Accident
Radionuclide Analysis on Bamboos following the Fukushima Nuclear Accident
Investigations on the radiocaesium contamination of wild boar (Sus scrofa) meat in Rhineland-Palatinate: a stomach content
analysis
The effect of heather burning on the transfer of radiocesium to smoke and the solubility of radiocesium associated withdifferent types of heather ash
Transuranic elements in ﬁshes compared to Cs-137 in certain lakes in Finland
Radiocesium transfer to man from moose and roe deer in Sweden
Radiocesium from chernobyl in Swedish moose
Chernobyl radioactivity persists in ﬁshRadiocesium (137CS) from the chernobyl reactor in eurasian woodcock and earthworms in Norway
Uptake of radiocesium by different species of mushrooms
Seasonal-variation in the activity concentration of Cs-137 in Swedish roe-deer and in their daily intake
Seasonal-variation in the activity concentration of cs-137 in Swedish roe-deer and in their daily intake
Transfer of Cs-137 to cows dairy product—investigations on dairy farms in sweden
Contamination of food in Czechoslovakia by cesium radioisotopes from the chernobyl accident
Cs-137 in Finnish wild berries, mushrooms and game meat in 2000–2005
Cs-137 in Finnish wild berries, mushrooms and game meat in 2000–2005
Cs-137 in Finnish wild berries, mushrooms and game meat in 2000–2005
Physiological and ecological factors inﬂuencing the radiocaesium contamination of ﬁsh species from Kiev reservoir
Speciﬁc cesium activity in fresh-water ﬁsh and the size effectEnvironmental-study of radioactive cesium in Greek lake ﬁsh after the chernobyl accident
137Cs, 239,240Pu and 241Am in boreal forest soil and their transfer into wild mushrooms and berries
137Cs, 239,240Pu and 241Am in boreal forest soil and their transfer into wild mushrooms and berries
Practical improvement of the radiological quality of dairy product produced by peasant farmers in the territories of Belarus
contaminated by the Chernobyl accident—The ETHOS project
Altitude dependent (Cs)-C-137 concentrations in different plant species in alpine agricultural areas
Altitude dependent (Cs)-C-137 concentrations in different plant species in alpine agricultural areas
Cs-137 and Sr-90 transfer to dairy product in Austrian alpine agriculture
Cs-137 and Sr-90 transfer to dairy product in Austrian alpine agriculture
Cesium concentration factors in wild herbivores and the fox (vulpes-vulpes l)
Ecological half-life of cesium in roe deer (capreolus-capreolus)

Dairy product
Dairy product
Tea

Fodder
Fish
Meat
Meat
Fish
Meat
Mushrooms
Meat
Meat
FodderDairy product
Meat
BerriesMushrooms
Fish
Fish
Fish
BerriesMushrooms
Dairy product
FodderFodderFodderDairy product
Meat
Meat

F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

Gattavecchia, E., Ghini, S., Tonelli, D.
Gilmore, B.J., Cranley, K.
Gorur, F.K., Keser, R., Akcay, N., Dizman, S., Okumusoglu,
N.T.
Grabowski, D., Muszynski, W.,
Petrykowska, M., Rubel, B., Smagala, G.,
Hakanson,
Lada, W. L., Andersson, T.
Hakanson, L.,
Hedvall, R., Erlandsson, B.
Heinrich
Henrich, E.

Table A2 (Continued)
Author

Year

Title

Group

Lux, D., Kammerer, L., Ruhm, W., Wirth,E.
Malinowska, E., Szefer, P., Bojanowski, R.
Marouf, B.A., Alhadad, A.K., Toma, N.A.,
Tawﬁq, N.F., Mahmood, J.A., Hasoon,
G., Franic, Z., Sencar, J., Bituh, T., Vugrinec, O.
Marovic,
M.A.
Martin, C.J., Heaton, B., Robb, J.D.

1995
1995
2006
1991
1991
2008
1988

Berries
BerriesMushrooms
Dairy productFoodstuff
Mushrooms
Meat

Mascanzoni, D.
Mascanzoni, D.
McGee, E.J., et al.

2009
1992
2000
2000
2000
1998
2010

Cycling of Pu, Sr, Cs, and other longliving radionuclides in forest ecosystems of the 30-km zone around Chernobyl
Cycling of Pu, Sr, Cs, and other longliving radionuclides in forest ecosystems of the 30-km zone around Chernobyl
Radionuclides content in Xerocomus badius and other commercial mushrooms from several regions of Poland
Radionuclide contamination of foods imported into Iraq following the chernobyl nuclear-reactor accident
Radionuclide contamination of foods imported into Iraq following the chernobyl nuclear-reactor accident
Mosses and Some Mushroom Species as Bioindicators of Radiocaesium Contamination and Risk Assessment
Studies of I-131, Cs-137 and Ru-103 in dairy product, meat and vegetables in North-east Scotland following the chernobyl
accident
Long-term transfer of Cs-137 from soil to mushrooms in a semi-natural environment
Determination of Sr-90 and Cs-137 in mushrooms following the chernobyl fallout
Chernobyl fallout in a Swedish spruce forest ecosystem
Chernobyl fallout in a Swedish spruce forest ecosystem
Chernobyl fallout in a Swedish spruce forest ecosystem
The inﬂuence of fungi on the long-term behaviour of radiocaesium in Norwegian sheep
Cs-137 and K-40 in fruiting bodies of different fungal species collected in a single forest in southern Poland
Radioactive contamination of Polish mushrooms
Radioactive contamination of Polish mushrooms
Chernobyl radioactivity in Turkish tea
Chernobyl radioactivity in Turkish tea
Long-term reduction of cesium concentration in dairy product after nuclear fallout
Trends in caesium activity concentrations in dairy product from agricultural and semi-natural environments after nuclear
fallout
Radioactive caesium deposition on rice, wheat, peach tree and soil after nuclear accident in Fukushima.
Dynamics of the radionuclide content in precipitation, grazing vegetation, and dairy product, in the leningrad region after theaccident at the chernobyl atomic-energy plant
Radiocesium Levels in Swedish Moose inRadioactivity in tobacco leaves
Seasonal variation in radiocaesium concentration in willow ptarmigan and rock ptarmigan in central Norway after the
Chernobyl fallout
Lower variability of radionuclide activities in upland dairy products compared to soils and vegetation: Implication forenvironmental survey
Lifetime accumulation of Cs-137 and K-40 in the ribs and sternum of an Austrian and ‘mountain pastureand’ cow
Original in Czech but mentioned in review of mushrooms (Kalac, 2001)
Short- and long-term patterns of Cs-137 in ﬁsh and other aquatic organisms of small forest lakes in southern Finland since theChernobyl accident
Analysis of radioactivity levels in soils and crops from the campania region (south Italy) after the chernobyl accident
Analysis of radioactivity levels in soils and crops from the campania region (south Italy) after the chernobyl accident
Analysis of radioactivity levels in soils and crops from the campania region (south Italy) after the chernobyl accident
Transfer of radiocesium from soil to vegetation and to grazing lambs in a mountain area in northern Sweden
Increased levels of cesium-137 and cesium-134 in 34 species of wild mushrooms following the chernobyl disaster
Evolution of radiocaesium contamination in ﬁshes after the Chernobyl accident
Evolution of radiocaesium contamination in ﬁshes after the Chernobyl accident
Evolution of radiocaesium contamination in ﬁshes after the Chernobyl accident
Cs 137 in freshwater and lake water in Finland after the Chernobyl deposition
Cs 137 in freshwater ﬁsh in Finland since 1986—a statistical analysis with multivariate linear regression models
Chernobyl-derived radiocesium in ﬁsh as dependent on water-quality and lake morphometry
Temporal changes in concentration of radiocaesium in lake sediment and ﬁsh of southern Finland as related to environmental
factors
Time-dependency of the Cs-137 contamination of wild boar from a region in Southern Germany in the years 1998 to 2009
Chernobyl radioactivity persists in reindeer
Chernobyl radioactivity persists in reindeer
Pollution— Chernobyland’s legacy in food and waterMushrooms
Mushrooms
Tea
Tea
Dairy product
Dairy product

Muck, K.
Muck, K., Gerzabek, M.H.

1994
1994
1990
1990
1995
1995

Nakanishi, T.M., Kobayashi, N.I., Tanoi, K.
Nedbaevskaya, N.A., Sanzharova, N.I., Blinova, L.D., II K,
Aleksakhin, R.M.
Palo et al.
Papastefanou, C.
Pedersen, H.C., Nybo, S., Varskog, P.

1991
2001
1998

Pourcelot, L., Steinmann, P., Froidevaux, P.

2007

Rabitsch, H., Pichl, E.
Randa et al.
Rask, M., Saxen, R., Ruuhijarvi, J., Arvola, L., Jarvinen, M.,
Koskelainen, U., Outola, I., Vuorinen, P.J.
Roca, V., Napolitano, M., Speranza, P.R.,
Gialanella, G.

2008
1993
2012

Rosen, K., Andersson, I., Lonsjo, H.
Ruckert, G., Diehl, J.F.
Ryabov, I.N., Belova, N.V., Polyakova,
N.I.
Saxén, R.L.
Saxén, R.L., Sundell, J.
Sarkka, J., Jamsa, A., Luukko, A.
Sarkka, J., Keskitalo, A., Luukko, A.
Semizhon, T., Putyrskaya, V., Zibold, G., Klemt, E.
Skuterud, L., Gaare, E., Eikelmann, I.M.,
Hove, K., Steinnes, E.
Smith, J.T., Comans, R.N.J., Beresford, N.A., Wright, S.M.,
Howard, B.J., Camplin, W.C.

2012
1991

1989
1989
1989
1995
1987
1998
1998
1998
2007
2006
1995
1996
2009
2005
2005
2000

FodderFodderMeat
TabaccoMeat
FodderMeat
Mushrooms
Fish

F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

Mehli, H., Skuterud, L.
Mietelski, J.W., Dubchak, S., Blazej, S., Anielska, T., Turnau,
K.
Mietelski JW, Jasinska M, Kubica B,
Kozak K, Macharski P
Molzahn, D., Tufail, M., Patzelt, P.

Mushrooms
Mushrooms
Mushrooms
Meat
Wood
Meat
Mushrooms

FodderFodderFood
Meat
Mushrooms
Fish
Fish
Fish
Fish
Fish
Fish
Fish
Meat
Meat
Meat
Fish

11

12

Table A2 (Continued)
Author

Year

Title

Group

Smith, J.T., Kudelsky, A.V., Ryabov, I.N.,
Hadderingh, R.H.

2000

Radiocaesium concentration factors of Chernobyl-contaminated ﬁsh: a study of the inﬂuence of potassium, and blind; testingof a previously developed model
Radiocaesium concentration factors of Chernobyl-contaminated ﬁsh: a study of the inﬂuence of potassium, and blind; testingof a previously developed model
Comparison of the postchernobyl Cs-137 contamination of mushrooms from Eastern-Europe, Sweden, and north-America
Comparison of the postchernobyl cs-137 contamination of mushrooms from eastern-Europe, Sweden, and north-America
Comparison of the postchernobyl cs-137 contamination of mushrooms from eastern-Europe, Sweden, and north-America
Land use inﬂuence on (137)Cs levels in perch (Perca ﬂuviatilis L.) and roach (Rutilus rutilus L.)
Transport of I-131 and Cs-137 from air to cows dairy product produced in north-western Italian farms following thechernobyl accident
Chernobyl and its radiological and socioeconomic consequences for the province of Salzburg, Austria
Chernobyl and its radiological and socioeconomic consequences for the province of Salzburg, Austria
Chernobyl and its radiological and socioeconomic consequences for the province of Salzburg, Austria
Inﬂuence of soil acidiﬁcation in southern Norway on the Cs-137 exposure of moose? Pages 3905–3908
Radiocesium in a Danish pine forest ecosystem
Radiocesium in a Danish pine forest ecosystem
Long-term trends in the uptake of radiocesium in Rozites caperatus
Cs-137-migration in soils and its transfer to roe deer in an Austrian forest standTime trends (1986–2003) of radiocesium transfer to roe deer and wild boar in two Austrian forest regions
Long-term dynamics of Chernobyl Cs-137 in freshwater ﬁsh: quantifying the effect of body size and trophic level

Fish

2000
Smith, M.L., Taylor, H.W., Sharma, H.D.

Sonesten, L.
Spezzano, P., Giacomelli, R.

Steinnes, E., Gaare, E., Engen, S.
Strandberg, M.
Strandberg, M.
Strebl, F., Gerzabek, M.H., Karg, V., Tataruch, F.
Strebl, F., Tataruch, F.
Sundbom, M., Meili, M., Andersson, E., Ostlund, M.,
Broberg, A.
Svadlenkova, M., Konecny, J., Smutny,
V.

1988
1988
1988
2009
1994
1994
2004
1996
2007
2003
1996
1996

Szanto, Z., Hult, M., Watjen, U.,
Altzitzoglou, T.
Teheranie
Thiry, Y., Colle, C., Yoschenko, V., Levchuk, S., Van Hees, M.,
Hurtevent, P., Kashparov, V.
Ugedal, O., Forseth, T., Jonsson, B., Njastad, O.
National Board of Atomic Safety and Radiation Protectionof the GDRVilic, M., Barisic, D., Kraljevic, P., Lulic, S.
Vinichuk, M., Rosen, K., Johanson, K.J., Dahlberg, A.

2007
2007
2007
1988
2009
1995
1988
2005
2011

Vinichuk, M., Taylor, A.F.S., Rosen, K., Johanson, K.J.

2010

Yoshida, S., Muramatsu, Y.
Yoshida, S., Muramatsu, Y., Dvornik,
A.M., Zhuchenko, T.A., Linkov, I.
Zibold, G., Drissner, J., Kaminski, S., Klemt, E., Miller, R.

1994
2004
2004
2001

Model calculation of radiocaesium transfer into food products in semi-natural forest ecosystems in the Czech Republic after anuclear reactor accident and an estimate of the population dose burden
Model calculation of radiocaesium transfer into food products in semi-natural forest ecosystems in the Czech Republic after anuclear reactor accident and an estimate of the population dose burden
Current radioactivity content of wild edible mushrooms: A candidate for an environmental reference material
Current radioactivity content of wild edible mushrooms: A candidate for an environmental reference material
Current radioactivity content of wild edible mushrooms: A candidate for an environmental reference material
Determination of 137Cs and 134Cs radioisotopes in various mushrooms from Austria one year after the chernobyl incident
Impact of Scots pine (Pinus sylvestris L.) plantings on long term Cs-137 and Sr-90 recycling from a waste burial site in the
Chernobyl Red Forest
Sources of variation in radiocesium levels between individual ﬁsh from a chernobyl contaminated Norwegian lake
Results of radiation monitoring in the German-democratic-republic after chernobyl(Cs)-C-137 concentration in meat of wild boars (Sus scrofa) in Croatia a decade and half after the Chernobyl accident
Correlations between potassium, rubidium and caesium (Cs-133 and Cs-137) in sporocarps of Suillus variegatus in a Swedish
boreal forest
Accumulation of potassium, rubidium and caesium (Cs-133 and Cs-137) in various fractions of soil and fungi in a Swedish
forestAccumulation of radiocesium in basidiomycetes collected from Japanese forests
Equilibrium of radiocesium with stable caesium within the biological cycle of contaminated forest ecosystems
Equilibrium of radiocesium with stable caesium within the biological cycle of contaminated forest ecosystems
Time-dependence of the radiocaesium contamination of roe deer: measurement and modelling

Mushrooms
Mushrooms
Mushrooms
Fish
Dairy product
Meat
Meat
Dairy productMeat
Mushrooms
Wood
Mushrooms
Meat
Meat
Fish
Mushrooms
MeatMushrooms
Mushrooms
Mushrooms
Mushrooms
Wood
Fish
Mushrooms
MeatMushrooms
Mushrooms
Mushrooms
Mushrooms
Wood
Meat

F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

Steinhausler, F., Hofmann, W., Daschil,F., Reubel, B.

1993
1993
1993
2001
1991

Fish

F. Gralla et al. / Ecological Indicators 41 (2014) 1–14

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