Journal of Environmental Radioactivity 158-159 (2016) 21e29

Contents lists available at ScienceDirect

Journal of Environmental Radioactivity
journal homepage: www.elsevier.com/locate/jenvrad

Review

Addressing ecological effects of radiation on populations andecosystems to improve protection of the environment against
radiation: Agreed statements from a Consensus Symposium*chignac a, b, *, Deborah Oughton c, Claire Mays d, Lawrence Barnthouse e,
François Bre
James C. Beasley f, Andrea Bonisoli-Alquati g, Clare Bradshaw h, Justin Brown i,phane Dray j, k, l, Stanislav Geras'kin m, Travis Glenn n, Kathy Higley o, Ken Ishida p,
Ste
Lawrence Kapustka q, Ulrik Kautsky r, Wendy Kuhne s, Michael Lynch t, Tapio Mappes u,
Steve Mihok v, Anders P. Møller w, Carmel Mothersill x, Timothy A. Mousseau y, Joji Otaki z,
Evgeny Pryakhin aa, Olin E. Rhodes Jr. ab, Brit Salbu c, Per Strand i, Hirofumi Tsukada acaInstitute for Radioprotection and Nuclear Safety (IRSN), Centre of Cadarache, BP 3, 13115 St Paul-lez-Durance, Cedex, France
International Union of Radioecology (IUR), Center of Cadarache, BP 3, 13115 St Paul-lez-Durance, Cedex, FranceCenter for Environmental Radioactivity (CERAD), Norwegian University of Life Sciences, P.O. Box 5003, 1432 Aas, NorwaydInstitut Symlog de France, 262 rue Saint-Jacques, 75005 Paris, Francee
LWB Environmental Services, Inc., 1620 New London Rd., Hamilton, OH 45013, USAf
University of Georgia, Savannah River Ecology Laboratory & Warnell School of Forestry and Natural Resources, PO Drawer E, Aiken, SC 29802, USAg
School of Renewable Natural Resources, Louisiana State University AgCenter, Baton Rouge, LA 70803, USAhDepartment of Ecology, Environment and Plant Sciences, Stockholm University, 10691 Stockholm, SwedeniNorwegian Radiation Protection Authority (NRPA), Østerås, Norwayj
Universit
e de Lyon, F-69000, Lyon, Francek
Universit
e Lyon 1, Francel
CNRS, UMR5558, Laboratoire de Biom
etrie et Biologie Evolutive, F-69622 Villeurbanne, FrancemRussian Institute of Radiology and Agroecology, Obninsk, RussianDepartment of Environmental Health Science, University of Georgia, Athens, GA 30602, USAoSchool of Nuclear Science and Engineering, Oregon State University, Corvallis, OR 97331, USAp
Graduate School of Agricultural and Life Sciences, The University of Tokyo, 113-8657, Japanq
LK Consultancy, P.O. Box 373, Turner Valley, Alberta T0L 2A0, Canadar
Swedish Nuclear Fuel and Waste Management Co., (SKB), P.O. Box 250, SE-101 24 Stockholm, Swedens
Savannah River National Laboratory, Aiken, SC, USAt
Department of Biology, Indiana University, 1001 East Third Street, Bloomington, IN 47405, USAu
Department of Biological and Environmental Science, University of Jyvaskyla, P.O. Box 35, 40014 Jyvaskyla, Finlandv
388 Church Street, Russell, Ontario K4R 1A8, Canadaw
Ecologie Syst
ematique Evolution, Universit
e Paris-Sud, CNRS, AgroParisTech, Universit
e Paris-Saclay, F-91405 Orsay, Cedex, Francex
Department of Medical Physics and Applied Radiation Sciences, McMaster University, Hamilton, Ontario, CanadayDepartment of Biological Sciences, and, the School of Earth, Ocean and Environment, University of South Carolina, Columbia, SC 29208, USAz
The BCPH Unit of Molecular Physiology, Department of Chemistry, Biology and Marine Science, Faculty of Science, University of the Ryukyus, Okinawa
903-0213, Japanaa
Urals Research Center for Radiation Medicine, Vorovsky Str. 68a, 454076 Chelyabinsk, Russiaab
Savannah River Ecology Laboratory (SREL), Drawer E, Aiken, SC 29802, USAac
Institute of Environmental Radioactivity, Fukushima University, 1 Kanayagawa, Fukushima-shi, Fukushima 960-1296, Japanbc*
Signatories, all of whom participated in the International Union of Radioecology 2015 Miami Consensus Symposium, endorse the agreed statements expressed in thispublication in their own names and under the aegis of the IUR. The responsibility of their respective institutions is not engaged.
* Corresponding author.
chignac), deborah.oughton@nmbu.no (D. Oughton), claire.mays@post.harvard.edu (C. Mays), barnthouse@lwb-env.
E-mail addresses: francois.brechignac@irsn.fr (F. Bre
com (L. Barnthouse), beasley@srel.uga.edu (J.C. Beasley), andreabonisoli@gmail.com (A. Bonisoli-Alquati), clare.bradshaw@su.se (C. Bradshaw), Justin.brown@nrpa.no(J. Brown), stephane.dray@univ-lyon1.fr (S. Dray), stgeraskin@gmail.com (S. Geras'kin), travisg@uga.edu (T. Glenn), kathryn.higley@oregonstate.edu (K. Higley), ishiken@
es.a.u-tokyo.ac.jp (K. Ishida), kapustka@xplornet.com (L. Kapustka), ulrikkauþiurj@gmail.com (U. Kautsky), wendy.kuhne@srnl.doe.gov (W. Kuhne), milynch@indiana.edu(M. Lynch), tapio.mappes@jyu.ﬁ (T. Mappes), smihok@bell.net (S. Mihok), anders.Moller@u-psud.fr (A.P. Møller), mothers@mcmaster.ca (C. Mothersill), mousseau@sc.edu(T.A. Mousseau), otaki@sci.u-ryukyu.ac.jp (J. Otaki), pryakhin@yandex.ru (E. Pryakhin), rhodes@srel.uga.edu (O.E. Rhodes), brit.salbu@nmbu.no (B. Salbu), per.strand@
nrpa.no (P. Strand), hirot@ipc.fukushima-u.ac.jp (H. Tsukada).

http://dx.doi.org/10.1016/j.jenvrad.2016.03.021
0265-931X/© 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

F. Brechignac et al. / Journal of Environmental Radioactivity 158-159 (2016) 21e29

22

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 24 March 2016
Accepted 26 March 2016

This paper reports the output of a consensus symposium organized by the International Union ofRadioecology in November 2015. The symposium gathered an academically diverse group of 30 scientists
to consider the still debated ecological impact of radiation on populations and ecosystems. Stimulated by
the Chernobyl and Fukushima disasters' accidental contamination of the environment, there is increasing
interest in developing environmental radiation protection frameworks. Scientiﬁc research conducted in avariety of laboratory and ﬁeld settings has improved our knowledge of the effects of ionizing radiation on
the environment. However, the results from such studies sometimes appear contradictory and there isdisagreement about the implications for risk assessment. The Symposium discussions therefore focusedon issues that might lead to different interpretations of the results, such as laboratory versus ﬁeld approaches, organism versus population and ecosystemic inference strategies, dose estimation approaches
and their signiﬁcance under chronic exposure conditions. The participating scientists, from across the
spectrum of disciplines and research areas, extending also beyond the traditional radioecology community, successfully developed a constructive spirit directed at understanding discrepancies. From thediscussions, the group has derived seven consensus statements related to environmental protection
against radiation, which are supplemented with some recommendations. Each of these statements is
contextualized and discussed in view of contributing to the orientation and integration of future
research, the results of which should yield better consensus on the ecological impact of radiation andconsolidate suitable approaches for efﬁcient radiological protection of the environment.
© 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Keywords:
Radiation effects
Ecological risk assessment
Populations
Ecosystems
Environmental protection
Consensus development

Contents
1.
2.
3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
Consensus statements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
Contextualizing the consensus statements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
3.1.
Protection goals; need for improved conceptualization and terminology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
3.1.1.
Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
3.2.
Linking field and laboratory studies and modeling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
3.2.1.
Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
3.3.
Realism, multiple stressors and confounding factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
3.3.1.
Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
3.4.
Dose and exposure characterization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
3.4.1.
Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
3.5.
Field study methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
3.5.1.
Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29

1. Introduction
Radiological protection is evolving from a system focused only
on humans, to one that encompasses non-human biota and theenvironment itself. In 2001, the International Union of Radioecology (IUR) arranged a Consensus Conference on Environmental
Radiological Protection which crystallized a broad agreement on
the need to address the environmental impacts of ionizing radiation (IUR, 2002a). Since then, scientiﬁc research in both the laboratory and the ﬁeld has signiﬁcantly improved our knowledge ofradiological impacts, yet there is a feeling of divergence rather thanconvergence in current opinion:
 Laboratory studies have reduced uncertainties related to impacts on individual non-human organisms, notably but not
exclusively through application of the reference organism
approach (IUR, 2000, 2002b; ICRP, 2003, 2008; FASSET, 2004;
ERICA, 2007; Sazykina and Kryshev, 2003, 2006) and thedevelopment of practical dose assessment tools. To assess risk to
non-human biota, various approaches use sophisticateddosimetry tools to estimate radiation dose to individuals andinfer the corresponding effects based on dose-response data
gathered from the literature. Considerable gains in knowledge
have been made in the last ten years through these initiatives.
However, the reference organism approach and other evolving
frameworks still need to be reﬁned for more realistic application
at the ecological level (Carroll, 2009; IUR, 2012; Bradshaw et al.,2014). For example, mainly acute exposure is studied in thelaboratory whereas the ﬁeld situation, even for humans, is oneof chronic exposure.
 Meanwhile, new information and increasing uncertainties haveemerged from recent ﬁeld studies, often conducted in areas
contaminated by nuclear accidents (e.g., Beresford andCopplestone, 2011; Murphy et al., 2011; Hiyama et al., 2012;
Geras'kin et al., 2013; Mousseau and Møller, 2014; Taira et al.,2014; Møller and Mousseau, 2015; Møller et al., 2015;
Deryabina et al., 2015; Pryakhin et al., 2016). These studies
have mostly focused on large-scale correlations among estimated exposures and natural history observations in the ﬁeld at
the level of individuals, populations, or of communities of

F. Brechignac et al. / Journal of Environmental Radioactivity 158-159 (2016) 21e29

species interacting within the ecosystem. Their ﬁndings sometimes appear to contradict predictions made under the traditional laboratory paradigm (Beresford et al., 2012). However,recent efforts have attempted to bridge the different approaches
and offered a number of explanations for divergence in ﬁndings(Garnier-Laplace et al., 2013, 2015).
Contrasted results from the laboratory and the ﬁeld, andresulting disagreement about their respective implications for risk
assessment and management, are currently stimulating a need forreﬁnement of international assumptions and ﬁndings relevant toenvironmental radiological protection systems (UNSCEAR, 2015).
Nuclear accidents, most recently the Fukushima disaster, provide astrong impetus to better address the very diverse situations andecosystems (potentially) affected by planned or unplanned releasesof ionizing radiation.
An ecocentric approach to environmental protection offers ameans for such reﬁnement, reconciling understanding of radiation
impacts developed mainly under acute exposure in the laboratory
with more recent observations under chronic exposure in the ﬁeld.
However, while there is increasing awareness of the need toembrace not only the individual level but also population, community and ecosystem impacts, radiation protection institutions
are only starting to engage the range of expertise that canconceptualize and conduct the relevant research. A new consensus
on the need and means to achieve an ecocentric approach might
stimulate dialogue, foster a more integrated research program, andfacilitate national and international efforts to work toward a morecomprehensive system of protection. More broadly, such consensus
might contribute to societal understanding of radioecology andgreater credibility in the eyes of decision makers, funding agencies,
and ultimately the public.
In this light, IUR launched a new consensus effort, with theintention to revisit the statement published in 2002, and to assess
the status of current research. A group of 30 scientists fromdifferent disciplines and research areas extending beyond the historical radioecology community came together for three days in
Miami in November 2015. They were invited to present and discuss
scientiﬁc work from the laboratory and the ﬁeld, identify areas ofagreement, explore reasons for disagreement about conceptual
approaches, and review different interpretations of the results aswell as their implications for environmental protection.
The 2015 Miami Consensus Symposium assembled scientists
from diverse areas of interest and perspectives who work withdifferent methods and points of reference. The group successfully
developed a constructive spirit directed at understanding discrepancies rather than arguing disagreements. This particularachievement allowed the formulation of seven statements, supported by observations and practical recommendations, whichhave been endorsed by the entire group.1
The seven consensus statements are gathered below, thencontextualized and developed in more detail. The program of presentations heard at the Miami Consensus Symposium, and notes on
the discussion questions and process, are provided in an appendix.
2. Consensus statements
Statement 1: Successful protection of the environment depends
on the protection of natural populations, their dynamics, species

1
One meeting participant does not appear among the authors because therequired employer validation procedure was judged to be prohibitively long. Thatparticipant, and one other, chose to endorse the seven statements presented hereby personally co-signing the short IUR note (2016) limited to those statements.

23

interactions and contributions to ecosystem functioning.
Ecosystem approaches are needed to support these protection
goals.
Statement 2: Improved terminology for referring to environmental protection criteria, operational outcomes and standardized methods is required.
Statement 3: Field studies and experiments, especially those
focusing on populations, make a vital contribution to the scientiﬁc background necessary to achieve the environmental
protection goals. Field data are essential to account for realistic
exposure scenarios, as well as to investigate how exposure toradionuclides interacts with other environmental factors todetermine the effects on natural populations.
Statement 4: Better continuity between laboratory and ﬁeld
studies should be developed to advance protection of theenvironment. Hypotheses should ideally be tested through an
iterative strategy integrating ﬁeld and laboratory studies, andmodeling efforts.
Statement 5: Strategies need to be developed to disentangle thedirect and indirect effects of radiation on (populations of) biota
in natural ecosystems, as well as the confounding factors thatprevent clear interpretation of the results.
Statement 6: Reference organism approaches represent an
important ﬁrst step to characterize doses to biota, but they havesigniﬁcant limitations. More effort should be placed on understanding mechanisms and processes of how radiation effects are
manifested in natural ecosystems, and on quantifying dose in
the ﬁeld.
Statement 7: Research programs and studies should encourage amultidisciplinary approach among radioecologists, radiobiologists, ecologists, evolutionary biologists, statisticians, modelers
and geneticists. Field study design should encompass methods
and approaches established in ecology and address a diverse
range of sites and cases with preferably experimental
approaches.

3. Contextualizing the consensus statements
3.1. Protection goals; need for improved conceptualization andterminology
It is now widely acknowledged that protection standards aimed
uniquely at humans do not necessarily ensure adequate protectionof non-human biota and related ecosystems (FASSET, 2004; ERICA,
2007; NEA, 2007). Moving away from the old paradigm assumingthat protection of man would ipso facto also protect the environment, IUR's 2001 consensus statement (IUR, 2002a) recognizedthat “man is part of the environment” but gave no detailed explanation of what this actually meant or implied. A better conceptualization of this statement is now needed.
A general conceptual model is proposed (Fig. 1) highlighting thefact that Homo sapiens is actually interacting with (and often outcompeting) other species within an ecosystem. Man is but one
predator species, while our agronomic species belong to ecologicalcategories such as primary producers (e.g., terrestrial plants) andprimary consumers (e.g., herbivorous mammals). Recognition of
the interdependency of man and other ecosystem components is aprerequisite for properly addressing how human and environmental radiological protection can be integrated.
Statement 1: Successful protection of the environment depends on the protection of natural populations, their dynamics, species interactions and contributions to ecosystem

24

F. Brechignac et al. / Journal of Environmental Radioactivity 158-159 (2016) 21e29

Fig. 1. “Man is part of the environment”: Conceptual model for a scenario of release of radioactivity to the air, integrating the various ecosystem components that include 1) abiotic
media (blue boxes), 2) various functional categories of wildlife accounting for primary producers (green boxes), primary consumers (yellow boxes), secondary consumers (orange
boxes), predators (brown box) and parasites (not shown) together with 3) Homo sapiens and companion agricultural species (red boxes), each being a subset of these ecologicalcategories. Arrows represent radionuclides transfer through these ecosystem components to top predators, highlighted in red when these are directed at H. sapiens. Depicting theecological relationships that link the natural trophic network for wildlife and the agronomic network for H. sapiens, this illustration indicates how man boosts ecological processeschignac, 2016).
toward his own food production by using herbicides and pesticides to outcompete natural populations (adapted from Breprocesses. Ecosystem approaches are needed to support these
protection goals.
There is a need for new methods and approaches to achieve thegoals of protecting not only H. sapiens, but also the ecosystems ofwhich humans are a part. The traditional approaches used today,
which largely rely on extrapolation from individual to population/
ecosystem level effects, are ﬂawed. Better approaches would
include direct consideration of population and ecosystem
attributes.
Recent ﬁeld studies on radiation effects demonstrate the limitations of exclusive reliance on models based solely on laboratory
experiments and methods based upon reference organisms. Thereis a difference between physiological (individual organismal level)
and ecological effects and between the consequences of these effects. Ecological effects include interactions at population level
among species and also between these species and their environment, potentially governed by emergent properties of these systems (Fig. 2). Because they lack ecological realism, models based on
ﬁndings from artiﬁcial laboratory contexts have been shown in atleast one case to be inaccurate in prediction by an order ofmagnitude (Garnier-Laplace et al., 2013). Similar phenomena havebeen seen in other ﬁelds of protection and the science of ecology as
a whole (Cairns et al., 1996; Newman, 2001; Tannenbaum, 2005).
Both physiology and ecology must inform environmental

protection frameworks, recognizing that these are inﬂuenced aswell by management systems, operational targets, philosophy,
politics, international context, etc. Understanding ecological effectsof radiation offers beneﬁts for environmental preparedness, environmental stewardship, remediation actions, science, increasing
credibility with the public, and putting radiation effects (of discharges, accidents, remediation, etc.) into context with other factors or effects.
To conclude, there is a need for environmental protection
criteria that reﬂect the dynamics and processes responsible forecosystem functioning (and resulting services). If protecting populations is a goal, methods and measurements must go beyond
individual effects. Ecological and evolutionary theories address
mechanisms that are highly relevant for generating realistic predictions of effects, and highlight the need for a new approach basedon systematic, long-term monitoring and study of real life
situations.
Statement 2: Improved terminology for referring to environmental protection criteria, operational outcomes and standardized methods is required.
Frameworks of environmental protection are being developedin areas outside the radiological protection ﬁeld: protection of
biodiversity, habitats, protection from physical/chemical stressors,
etc. The supporting terminology comes essentially from ecology

F. Brechignac et al. / Journal of Environmental Radioactivity 158-159 (2016) 21e29

25

Fig. 2. Different targets of protection require proper alignment of the corresponding methodological approaches designed to achieve the associated goals. Reference organism
approaches are mismatched with respect to protection goals set at population and ecosystem levels; these latter require development of ecosystem-oriented approaches. The
former are usually supported by laboratory experiments whilst the latter can use laboratory and ﬁeld micro- and mesocosm experiments as well as ﬁeld measurements andexperiments, to support this orientation (adapted from Bradshaw et al., 2014).

and environmental sciences regarding non-radiological stressors(chemicals, etc.). Radioecology should adopt the right terminologies in the right context to avoid errors and imprecision. “Objects,
targets, endpoints” may have different meanings depending on the
different levels of inquiry (measurement, assessment, etc.).
Our use of terminology must be sufﬁciently precise to help us
identify gaps. For instance, the term “environmental protection” iswidely used for current radiological protection systems (ICRP, 2003,
2008). In practice however, current approaches protect species onlyat the organismal level stricto sensu. Furthermore, abiotic media(i.e. air, water, soils and sediments) which form important components of the environment subject to potential contamination are
not expressly covered by these systems.
The increasingly cited concept of “ecosystem services” may aid
in highlighting humans' dependence on the environment. This
notion stemming from an anthropocentric vision may prove to be
an important communication tool. However, work needs to be
carried out to determine how it can or should be implemented inradiological protection of the environment (Morelli and Møller,2015).
3.1.1. Recommendations
 Ecosystem approaches need to be supported by systems-levelresearch emphasizing interactive responses to radiation exposure, propagation of effects, delayed effects, indirect effects, andchignac
resistance and resilience of ecological systems (e.g. Bre
et al., 2011).
 Environmental protection criteria to be developed should
consider population and ecosystem attributes involving more
integrated and functional endpoints such as population

dynamics, biodiversity, decomposition, primary productivity,
energy transfer or nutrient ﬂow.
3.2. Linking ﬁeld and laboratory studies and modeling
Both ﬁeld and laboratory studies are needed to form the scientiﬁc basis for environmental assessments. These should becomplementary and largely co-constructed to improve the overall
analytical power, but need not have the same objectives, methods
or endpoints.
Statement 3: Field studies and experiments, especially those
focusing on populations, make a vital contribution to the scientiﬁc background necessary to achieve the environmental
protection goals. Field data are essential to account for realistic exposure scenarios, as well as to investigate how exposure
to radionuclides interacts with other environmental factors todetermine the effects on natural populations.
Field studies focusing on species assemblages are essential toaccount for variation across species and higher-level taxa in
exposure, sensitivity, and response to radioactive contaminants incombination with other stressors. Although entangled in various
functional groups of ecosystems, natural populations and their individuals in their ecological settings are the fundamental units forinvestigating expected consequences of radiological contamination. These include both direct and indirect consequences mediatedby effects on other interacting species and/or trophic levels. Field
studies are usually characterized by lower statistical power,
therefore delivering less certainty about causes and effects, butthey beneﬁt from higher ecological relevance.

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F. Brechignac et al. / Journal of Environmental Radioactivity 158-159 (2016) 21e29

Fig. 3. Hypothesis-driven inference strategy linking laboratory experiments, ﬁeld studies and modeling. Potential contributions of each approach to advancing protection of theenvironment are shown, as well as links between the different stages of the proposed iterative strategy. The circular shape is used to represent interconnectedness and reciprocal(two-way) feedback between the different stages and approaches. Shortcomings of each approach that can be resolved by resorting to a different methodology are indicated in red.

Laboratory experiments are fundamental tools that contributeto environmental protection. Thanks to their simpliﬁed and more
controlled nature, laboratory experiments provide mechanistic
insights into pathways of exposure and translation of exposure tobiological effects at the genetic, cytogenetic and physiologicallevels. Laboratory experiments should help to clarify if such effects
are purely physiological, meaning that they do not persist overgenerations, or if they arise from permanent mutational genome
damage, that is harder to eliminate. Laboratory studies haveallowed the development of methods of quantiﬁcation of exposure
to radiation, a database on dose-effect relationships in organisms(Copplestone et al., 2008), and a conceptual approach to risk
assessment based on biological effects of radiation (similarly as forhumans). They usually suffer from poorer ecological relevance, but
beneﬁt from clearer outcomes and higher statistical power.
It is to be stressed that ﬁeld studies are generally based on
chronic exposure, while laboratory studies usually use acuteexposure. This creates a dichotomy that may be part of an explanation for the different conclusions drawn from ﬁeld and laboratory studies.
Modeling is also an approach of high importance due to its capacity to support data testing and assimilation along an integrated
ecosystem conceptual model. Microcosms and mesocosms play an
integral role in linking laboratory and ﬁeld studies in ecology(Odum, 1984). Such experimental systems provide an important
middle-ground, allowing replication of experiments in seminatural scenarios, but with fewer confounding variables. Recent
combination of mechanistic modeling with model-guided experiments in a microcosm has proved very helpful in understanding thestressors' effects on this simpliﬁed ecosystem functioning(Lamonica et al., 2016).
In order to advance understanding of radiation ecological impacts on the environment, better links should be made between
ﬁeld, laboratory and modeling studies, using an iterative andhypothesis-driven process (Fig. 3).
Several examples of such linkages that recently proved successful in supporting better interpretation can be mentioned.

Garnier-Laplace et al. (2015) showed a high degree of consistency
between dose measurements in the ﬁeld and calculated dose estimates based on morphology, diet and ecology of birds at
Fukushima. Otaki and coworkers (Hiyama et al., 2012; Taira et al.,2014) supported convincingly their hypothesis drawn from ﬁeld
observations that radiation induced mutations in the pale grassbutterﬂy, when they obtained similar mutations in laboratorybased experiments under controlled conditions where the only
variable was radiation.
Statement 4: Better continuity between laboratory and ﬁeld
studies should be developed to advance protection of theenvironment. Hypotheses should ideally be tested through an
iterative strategy integrating ﬁeld and laboratory studies, andmodeling efforts.

3.2.1. Recommendations
 Contaminated sites have been subjected to long-term monitoring and observations but the extent and level of research isextremely limited compared to standard procedures in ecology.
Surprisingly, there are few monitoring studies of the mostcommon taxa at Chernobyl, Fukushima, Mayak and elsewhere.
Long-term monitoring studies have been restricted to a few ﬁeld
studies at Chernobyl and Fukushima during the last decade. It ishighly desirable to initiate and maintain annual monitoringstudies of all common taxa at representative sites mostcontaminated by major accidental releases of radioactivity into
the environment. The challenge here would be to carry out ﬁeld
experiments with a decent level of replication.
 The next step should be the development of ecosystem conceptual models, depicting networks of interactions and systems
to generate hypotheses about nodes/pathways/sub-networks
seen as important. This modeling effort could provide acomprehensive and integrated picture of observed radiation

F. Brechignac et al. / Journal of Environmental Radioactivity 158-159 (2016) 21e29

biological/ecological effects, to be confronted with real data, andultimately yielding an improved understanding.
 Such conceptual models could then be further supplemented by
microcosm and mesocosm studies to help bridge the gap between ﬁeld and laboratory studies. Overall, this would enable
the use and integration of genetics and other biological tools/
approaches in the more applied ecological investigations,informing ecology with genetics and physiology. Likewise,
studies of epigenetics will provide information on patterns ofmethylation and other effects affecting the expression of genes.
3.3. Realism, multiple stressors and confounding factors
Multiple types of biological and ecological effects have been
revealed by observational ﬁeld studies at sites with elevated levelsof radiation. Field experiments, however, are challenging to design
and interpret, due to many potentially confounding variables suchas diet, habitat, predator stress, biological stressors (parasites),presence or absence of competitors (including humans), abiotic
factors (e.g. temperature, pH), hot spots of contamination, indirect
and direct effects of exposure and exposure type (radionuclides,
metals, chemicals, etc.).
Statement 5: Strategies need to be developed to disentangle thedirect and indirect effects of radiation on (populations of)biota in natural ecosystems, as well as the confounding factorsthat prevent clear interpretation of the results.
Signiﬁcant work remains to link ﬁeld studies and ecosystemproperties with updated and improved datasets on radiation effects. Whereas recent laboratory-based experiments by the radioecology community have assembled a database of radiation effects
on organisms of various species, its robustness suffers from lack ofreplication and inclusion criteria that are still sometimes subject tocriticism. Commensurable effort should be invested in developing a
database of radiation impact observations from ﬁeld studies,
especially for population- and ecosystem-related endpoints.
When disagreements, however, remain on the degree to whichﬁeld observations can be attributed to radiation effects, the iterative hypothesis-driven inference strategy recommended above(Statement 4) together with efforts of independent replication
should help resolve confounding factors. Basically, this is a questionof setting up an appropriate experimental design (Møller andMousseau, 2016).
3.3.1. Recommendations
 It is important to consider the interconnectedness of species,
investigating interspeciﬁc interactions, as well as designing ﬁeld
studies that integrate different trophic levels and look at higher
ecosystem levels.
 The design of future ﬁeld experiments should also consider
testing and replication of published information on chemical or
metal exposure and effects on species in ecosystems of interest.
 Attention should be dedicated to making use of experimental
designs and statistical methods that are most appropriate toresolving confounding factors.
3.4. Dose and exposure characterization
There is an ongoing need to improve the measurement ofenvironmentally relevant exposures, particularly under multiple
sources of exposure from different types of radionuclides and otherstressors. The quantiﬁcation of exposure to radiation still accounts
for a large portion of the uncertainty affecting risk assessment. Both27

dose rate and total accumulated dose (over the whole life span, andespecially at low dose rates) need to be addressed, with a further
focus on sensitive life stages (e.g. developmental and reproductive
life stages, looking in particular at gametes and embryos).
Assessment of dose to tissues and organs is still poorly developed for non-human biota. This limits the analytic power of bothlaboratory and ﬁeld studies, due to the fact that such tissues andorgans may have widely different radiosensitivities, and/or could
accumulate radionuclides to differing degrees.
Dose and exposure characterization are essential for reference
organism approaches which relate dose to biological effects at thegenetic, cytogenetic, physiological, cellular and individual levels.
Such approaches based upon biology can help at early stages andmesh with existing systems focused on humans. However, protection of ecosystems clearly requires a system-level inference
strategy and associated methodology.
Statement 6: Reference organism approaches represent an
important ﬁrst step to characterize doses to biota, but they
have signiﬁcant limitations. More effort should be placed onunderstanding mechanisms and processes of how radiation
effects are manifested in natural ecosystems, and on quantifying dose in the ﬁeld.
Considering high level emergent properties of ecosystems suchas resilience, it is doubtful that a universal standard (dose or doserate) suitable for protection of any ecosystem can be established.
Each ecosystem has its particular level of resilience at any time andexperiences a variety of concomitant stressors. Due to the very
multi-dimensional character of ecosystems in which combined andindirect effects produce a cascade of outcomes, the most serious
effects may not result from ionizing radiation alone but from its
combination with other factors. In such a case, ionizing radiation
would then only act as a trigger promoting ecological disruption.
Accounting for such a disruption mechanism at the system level
requires consideration of endpoints operating at the ecosystemlevel (ecosystem structure, ecosystem functioning).

3.4.1. Recommendations
 A better knowledge of the relative radiosensitivities of different
species and endpoints will allow us to understand and predictthe mechanisms underlying interspecies interactions in an
irradiated ecosystem. The time is now ripe to revisit the chart ofradiosensitivity across the kingdom of life (Whicker and Schultz,
1982). It has often been cited as a demonstration that radiosensitivity increases together with complexity of life (fromunicellular bacteria up to higher levels of organization such as
mammals). However, radiosensitivity also varies according to
the endpoint through which it is measured (Copplestone et al.,2008). There are today sufﬁcient data collected for many species both on organism-related endpoints (laboratory experiments) and individual or population endpoints, to enable theconstruction of (different) scales of radiosensitivity for eachindividual endpoint (or category of related endpoints withsimilar responses) (e.g. literature reviewed to assemble the
ERICA (Real et al., 2004) and EPIC (Sazykina and Kryshev, 2003,
2006) data bases, as well as unpublished grey literatureassembled in nuclear industrial/research sites).
 Improved efforts of quantifying dose (dose rate and accumulated dose) are warranted, especially for ﬁeld experiments
where exposure is usually complex (different radiation types,
different routes of internal/external exposure, different radiosensitivities across the life cycle of organisms).

F. Brechignac et al. / Journal of Environmental Radioactivity 158-159 (2016) 21e29

28

3.5. Field study methods
Much of the recent ﬁeld work tends to focus on single accidental
releases. The historical reasons for this are understandable, and it
must also be acknowledged that methodological approaches inﬁeld ecology and other disciplines may differ. An approach that
integrates ﬁeld and laboratory studies would increase comprehension between the disciplines, and probably also help morescientiﬁc conﬁdence and more funding for important ﬁeld studies.
For example, screening of biological communities for the collectionof measurements and samples should integrate with developments
in dose reconstruction and characterization, in order to clarify
variation across species in exposure or sensitivity.
Statement 7: Research programs and studies should encouragea multidisciplinary approach among radioecologists, radiobiologists, ecologists, evolutionary biologists, statisticians,modelers and geneticists. Field study design should encompass
methods and approaches established in ecology and address adiverse range of sites and cases with preferably experimental
approaches.
It is possible to conduct experimental ﬁeld studies capable ofestablishing a sufﬁcient level of conﬁdence and consensus in thelikely cause-effect relationship of radiation effects in ecosystems.
This requires increasing collaboration between different disciplines, with regard also to identifying the endpoints to be analyzed
and the number and types of sites to be investigated.
Field studies are most generally conducted by ecologists who
rely on observations, experiments and associated measurements in
the real environment. There is a wide array of possible andnecessary methods (contamination conditions, endpoints, etc.) thatallow ﬁeld studies to yield correlations but also causality between
radiation and potential effects. Ecosystem level endpoints could
include keystone species/groups (nodes) and key ecosystem processes (links) appropriate to the ecosystem in question (e.g. structural and functional endpoints). Though this appears conceptuallyattractive, there are practical aspects to consider and resolve before
application.
Substantial environmental monitoring of radiation is conductedby operators in the vicinity of nuclear power plants. Currently, thedata generated are insufﬁcient to support complex ecosystem
studies and protection, largely because environmental levels tend
not to be recorded if they lie below the set detection level, or if the
instruments in use are limited (e.g. detecting external gamma radiation only). End of pipe or close to stack releases can be measured
and used to model environmental levels but cannot function for
legacy sites or post-accidental situations. However, provided thereis improved cooperation between researchers and operators, suchenvironmental monitoring could be expanded to deliver additional
useful observations (ecosystem structure and functions), to establish the normal range of criteria of interest, and enable development of a list of reference ecosystems.

3.5.1. Recommendations
 A wider variety of sites, presenting different ecosystem situations with complex variables, should be exploited to advanceour understanding of radiation effects at population andecosystem levels and how these are mediated through biological effects at the organismal level. The sites of particular relevance are:
 Accidentally contaminated sites (Kyshtim, Chernobyl,
Fukushima, etc.).

 Legacy sites (Mayak, Kola Peninsula, Semipalatinsk, Paciﬁcatolls, etc.).
 Sites with a high level of natural radioactivity (Kerala, Poças deCaldas, Komi).
 Well characterized sites, which may include: uranium mining
sites; US DOE sites; gas and oil sites; marine sites receiving
exhaust pipes; former test sites; waste management/waste
disposal sites.
 Sites with already existing monitoring programs and otherhistorical databases that could complement the gathering of
new information; pertinent existing observatories and noncontaminated sites.
 In addition to widening the scope of sites of interest, a renewed
effort of historical data assembly and mining should be carriedout, accessing the Russian, Ukrainian and Belarussian literature,
the grey literature and other unpublished government and industry reports.
4. Conclusions
To assess (and manage) radiological risk at the ecological level
responds to ethical imperatives from several perspectives, and canbe regarded as a duty both to human society and to the ecosystemsof which we are a part (IAEA, 2002; Oughton, 2003; IUR, 2012).
Proper risk assessment, and subsequent management, requires
both an appropriate understanding and a convincing and appropriate system of environmental protection. In this context, promoting shared understanding within the scientiﬁc community
regarding the occurrence of ecological impacts of radiation is ofhigh strategic importance. In particular, the still on-going debate onwhether or not the Chernobyl and Fukushima accidents are having
ecological consequences needs to be resolved (Beresford andCopplestone, 2011; Hiyama et al., 2012; Geras'kin et al., 2013;
Møller and Mousseau, 2015, 2016; Taira et al., 2014). Suspicion byscientists as to results obtained outside their own chapel, and lackof consensus about assessing and interpreting risk, may jeopardize
the radioecology community's credibility in the eyes of decision
makers and funding agencies, and ultimately the public. Further tothe early consensus statement elaborated 15 years ago (IUR,
2002a), the Miami Consensus Symposium has constructed a new
set of collectively agreed statements about means to assess theecological impact of radiation and their conceptual implications fordesigning environmental protection.
The Miami statements urge in particular a better effort to create
linkage between controlled experimentation in the laboratory andin situ studies. At present these are often carried out by different
scientists, or groups of scientists, educated in separate disciplineschignac, 2005). All apply their respective con(see Hinton and Bre
ceptual and methodological approaches which do not look, forexample, at the same endpoints. Generally speaking, laboratory
scientists look at biological effects (interaction of radiation withmolecules, cells, tissues, and individual organisms) while ﬁeld
scientists look at ecological impact of radiation on individuals andpopulations of species interacting with populations of other taxa
and hence constituting ecosystems. This cultural gap largely explains why respective scientiﬁc communities have so far largely
operated in isolation from one another. Collective consensus is now
being expressed that further research should no longer suffer fromthis historical weakness, and a strategy for broader collaborationand coordinated work is strongly encouraged.
The Miami discussion also emphasized that ecosystem approaches provide a unifying conceptual basis: for linking laboratory
and ﬁeld studies, for assembling human and environmental
radiological protection in a justiﬁed and coherent manner, and for
integrating scientiﬁc understanding gained at various levels,

F. Brechignac et al. / Journal of Environmental Radioactivity 158-159 (2016) 21e29

analytic as well as systemic, toward the goal of assessing ecologicalrisk in situ while ultimately providing better protection.
Acknowledgement
The authors wish to thank Dr Armelle Guilloux (Ellipse&Co) for
the warm ambiance and excellent logistics organization of the 2015
Miami International Consensus Symposium.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jenvrad.2016.03.021.
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