Radioecology for boreal ecosystems : studies on transfer processes and effects on wildlife

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Dissertations in Forestry and Natural Sciences

DISSERTATIONS | SOROUSH MAJLESI | RADIOECOLOGY FOR BOREAL ECOSYSTEMS: STUDIES ON TRANSFER PROCESSES ... | No 432

SOROUSH MAJLESI

Radioecology for Boreal Ecosystems:

Studies on Transfer Processes and Effects on Wildlife

PUBLICATIONS OF

THE UNIVERSITY OF EASTERN FINLAND

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RADIOECOLOGY FOR BOREAL ECO- SYSTEMS: STUDIES ON TRANSFER PROCESSES AND EFFECTS ON WILD-

LIFE

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Soroush Majlesi

RADIOECOLOGY FOR BOREAL ECO- SYSTEMS: STUDIES ON TRANSFER PROCESSES AND EFFECTS ON WILD-

LIFE

Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences

No 432

University of Eastern Finland Kuopio

2021

Academic dissertation

To be presented by permission of the Faculty of Science and Forestry for public examination in the Auditorium SN200 in the Snellmania Building at the University of Eastern Finland, Kuopio, on November, 12,

2021, at 12 o’clock noon

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Punamusta Oy Joensuu, 2021 Editor: Pertti Pasanen

Distribution: University of Eastern Finland / Sales of publications www.uef.fi/kirjasto

ISBN: 978-952-61-4307-1 (nid.) ISBN: 978-952-61-4308-8 (PDF)

ISSNL: 1798-5668 ISSN: 1798-5668 ISSN: 1798-5676 (PDF)

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Author’s address: Soroush Majlesi

University of Eastern Finland

Depart. of Environmental and Biological Sciences P.O. Box 1627

70211 KUOPIO, FINLAND email: soroush.majlesi@uef.fi

Supervisors: Professor (emer.) Jukka Juutilainen, Ph.D.

70211 KUOPIO, FINLAND email: jukka.juutilainen@uef.fi

Associate Professor Jonne Naarala, Ph.D.

70211 KUOPIO, FINLAND email: jonne.naarala@uef.fi

Dr. Christina Biasi, Ph.D.

70211 KUOPIO, FINLAND email: christina.biasi@uef.fi

Dr. Jarkko Akkanen, Ph.D.

80101 JOENSUU, FINLAND email: jarkko.akkanen@uef.fi

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Reviewers: Professor Gareth Law, Ph.D.

University of Helsinki Depart. of Chemistry PL 55 (A. I. Virtasen aukio 1) 00014 HELSINKI, FINLAND email: gareth.law@helsinki.fi Professor Nick Ostle, Ph.D.

Lancaster University

Lancaster Environment Centre Lancaster, United Kingdom email: n.ostle@lancaster.ac.uk Opponent: Professor Clare Bradshaw, Ph.D.

Stockholm University

Dept. of Ecology, Environment and Plant Sciences Stockholm, Sweden

email: clare.bradshaw@su.se

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7 Majlesi, Soroush

Title of the thesis. Radioecology for boreal ecosystems: studies on transfer processes and effects on wildlife

Kuopio: University of Eastern Finland, 2021 Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences 2021; 432 ISBN: 978-952-61-4307-1 (print)

ISSNL: 1798-5668 ISSN: 1798-5668

ISBN: 978-952-61-4308-8 (PDF) ISSN: 1798-5676 (PDF)

ABSTRACT

Nuclear power is an important source of energy and a means to decrease the use of fossil fuels and to manage the climate crisis. One of the main challenges of this technology, however, is management of radioactive waste that could be released into the biosphere. Radionuclides, released into the environment due to poor management of radioactive waste, may incorporate into various environmental components and be assimilated by flora and fauna as parts of the food web. This study focused on understanding the transfer of radionuclides in aquatic and terrestrial ecosystems as well as on possible effects on the wildlife.

Transfer of ¹⁴C from soil to two plant species was investigated on a peatland site by using a novel approach to distinguish between soil and atmosphere as sources of C.

The aim of this study was to determine the contribution of soil-derived C to plant C on a site where a large difference in ¹⁴C/total C ratio between modern air and up to 8000-year leftover peat exists. This yields an ideal opportunity to track the contribution of atmospheric C and soil-derived C in plants growing on the peatland. The results showed higher contribution of soil C in plant roots (up to 5%), while no contribution was observed in above-ground parts despite up to 14% of soil-derived C being available in the canopy. The findings suggested that ¹⁴C possibly released from radioactive waste has low potential to further distribute to above-ground parts of the biosphere, which is mainly supported by plants through photosynthesis.

Transfer of Cl, Co, Mo, Ni, Se, Sr, U and Zn into freshwater species, chironomid larvae (Chironomus sp.), roach (Rutilus rutilus) and perch (Perca fluviatilis) was investigated in three ponds. These elements are important in safety assessment of radioactive waste. The study was carried out at two ponds near a former uranium mine and a reference pond, located further away from the mining area. Overall, the concentration of elements in media and biota and animal-to-water/sediment concentra-

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tion ratios suggested that sediment was the main source of uptake except for Cl.

This finding should be considered in radioecological models, especially in boreal aquatic ecosystems rich in organic matter. The results also suggested that, while the transfer of elements into chironomid larvae may be linear, such assumption is not valid for fish species.

Finally, possible developmental effects of uranium mine-affected sediments on non- biting midges, Chironomus riparius were investigated in a microcosm study. The approach used in this study based on exposure of laboratory-reared animals were exposed to sediments collected from the field from the same ponds that were the basis of the transfer studies. This approach helps to avoid confounding variables in the environment and adaptation of field organisms to long-term contamination.

The results revealed no fluctuating asymmetry in length of wing veins in adult chironomids. However, time to emergence differed significantly between control and U-contaminated treatments, questioning the conjecture that measurement of fluctuating asymmetry is particularly sensitive in detecting effects of low-level contamination.

The results of this work are expected to be useful in further development of current radioecological models relevant to boreal ecosystems and assessment of possible risks to the biosphere.

Universal Decimal Classification: 504.5, 504.61, 539.163, 574.4, 574.58, 621.039.7, 628.4.047

CAB Thesaurus: nuclear energy; nuclear power stations; radioactive wastes; radionuclides;

ionizing radiation; transfer; cold zones; wildlife; carbon; peatlands; soil; peat; plants; roots;

uptake; leaves; canopy; Pinus sylvestris; mycorrhizas; chlorine; cobalt; molybdenum; nickel;

selenium; strontium; uranium; zinc; ecosystems; aquatic environment; aquatic communities; food chains; Chironomus; larvae; fishes; Rutilus rutilus; Perca fluviatilis;

mining; ponds; concentration; water; sediment; benthos; biota; organic matter; models Yleinen suomalainen ontologia: ydinenergia; ydinvoimalat; ydinjätteet; radioaktiiviset jätteet; nuklidit; hiili; kloori; koboltti; molybdeeni; nikkeli; seleeni; strontium; uraani; sinkki (metallit); kertyminen; boreaalinen vyöhyke; ekosysteemit (ekologia); villieläimet;

ravintoketjut; turvemaat; kasvit; metsämänty; vesiekosysteemit; vesieläimistö; kalat; särki;

ahven; surviaissääsket; toukat; sedimentit; pohjaeliöstö; orgaaninen aines; mallit (mallintaminen)

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9 ‘’Out beyond ideas of wrongdoing and rightdoing there is a field. I’ll meet you there.

When the soul lies down in that grass, the world is too full to talk about’’

Rumi

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ACKNOWLEDGEMENTS

This PhD thesis was carried out during the years 2017-2021 in Radiation and Chem- icals Research Group, Department of Environmental and Biological Sciences, Uni- versity of Eastern Finland. The work was financially supported by the Finnish Re- search Programmes on Nuclear Waste Management (KYT 2018 and KYT 2022) and a stipend from the University of Eastern Finland.

First of all, I would like to thank my principal supervisor, Professor emeritus Jukka Juutilainen for providing me the opportunity to start my academic career. His kindness, support, and thoughtful comments motivated me during my PhD study.

I also would like to thank my other supervisors, Dr. Jarkko Akkanen, Associate Professor Jonne Naarala and Dr. Christina Biasi for their contribution to this work.

I am very much thankful to Associate Professor Jouni Sorvari for all his assistance to the experiment and the statistical analyses in chapter 4. His contribution is very acknowledged. I am also grateful to the discussions and valuable comments of Dr.

Päivi Roivainen.

I would like to express my gratitude to the official reviewers of the thesis, Professor Nick Ostle and Professor Gareth Law for their critical comments. I wish to also thank Professor Clare Bradshaw for acting as my opponent.

I am truly honored to dedicate this thesis to my lovely parents, my sister, Mitra and my brother, Arash whose presence inspires me to grow as a person through hard- ships and challenges of my life. Without your support it wouldn’t be possible.

Finally, I would like to express my deepest appreciation to my wonderful wife, Zahra, for her endless love and support and for being the sweetest gift of my life.

Kuopio, September 2021 Soroush Majlesi

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LIST OF ABBREVIATIONS

AFW Artificial freshwater

AMAP Arctic Monitoring and Assessment Programm AMS Accelerator mass spectrometer

AVS Acid-volatile sulfides β Beta

BL Biotic ligand BLM Biotic ligand model

Bq Becquerel

Bq g^-1 Becquerel per gram Bq kg^-1 Becquerel per kilogram CBR Critical body residue CEC Cation exchange capacity Ci km^-2 Curie per square kilometer C kg-1 Coulomb per kilogram CR Concentration ratio DA Directional asymmetry Dext External dose

Dint Internal dose

DIC Dissolved inorganic carbon DOC Dissolved organic carbon DOE U.S. Department of Energy DOM Dissolved organic matter

DW Dry weight

E Energy

EEM Exposure-effects model FA Fluctuating asymmetry

FL Feeding level

foc Fraction of organic carbon

FW Fresh weight

g kg^-1 Gram per kilogram g mL^-1 Gram per millilitre Gy Gray

ha Hectare

IAEA The International Atomic Energy Agency

ICRP International Commission on Radiological Protection IRSN Institut de radioprotection et de sûreté nucléaire Jkg-1 Joule per kilogram

kBq m^-2 Kilobecquerel per sqare meter

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KBS Kärnbränslesäkerhet Kd Distribution coefficient

Km Kilometer

LBC Lethal body concentration L kg^-1 Litre per kilogram

LMM Low molecular mass

M Molar

m Meter

mL Millilitre

mg kg^-1 Milligram per kilogram mg L^-1 Milligram per liter

MOB Methane-oxidizing bacteria

NE Northeast

NOEC No observed effect concentrations

OECD The Organisation for Economic Co-operation and Development PAH polycyclic aromatic hydrocarbons

pMC Percent modern carbon

PNEC Predicted no effect concentration R Roentgen

POC Particulate organic carbon RCG Reed canary grass

ROS Reactive oxygen species sBLM Sediment biotic ligand model SEM Simultaneously extracted metals SI International System of Units SKB Svensk Kärnbränslehantering Ab Sv Sievert

µg L^-1 Microgram per litre µGyh^-1 Microgray per hour

µL Microlitre

µm Micrometer

µS cm^-1 microSiemens per centimeter µSv h^-1 Microsievert per hour

UNSCEAR United Nations Scientific Committee on the Effects of Atomic Radiation

UO22+ Uranyl ion

Wm^-2 Watt per square meter

yr Year

ZnO Zinc oxide

x Absorbed fraction

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LIST OF ORIGINAL PUBLICATIONS

This thesis is based on data presented in the following articles, referrred to by the Roman Numerals I-III.

I Majlesi, S., Juutilainen, J., Kasurinen, A., Mpamah, P., Trubnikova, T., Oinonen, M., Martikainen, P. and Biasi, C., (2019). Uptake of Soil-Derived Carbon into Plants: Implications for Disposal of Nuclear Waste. Environmental Science & Technology, 53(8): 4198-4205.

II Majlesi, S., Akkanen, J., Roivainen, P., Tuovinen, T.S., Sorvari, J., Naarala, J. and Juutilainen, J., (2021). Transfer of elements relevant to radioactive waste into chironomids and fish in boreal freshwater bodies. Science of The Total

Environment, 791, 148218.

III Majlesi, S., Carrasco-Navarro, V., Sorvari, J., Panzuto, S., Naarala, J., Akkanen, J. and Juutilainen, J., (2020). Is developmental instability in chironomids a

sensitive endpoint for testing uranium mine-affected sediments?. Science of The Total Environment, 720, 137496.

The original articles have been reproduced here with the kind permission of the copyright owners.

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AUTRHOR’S CONTRIBUTION

I) Soroush Majlesi performed the data analysis and wrote the draft of the manuscript. Promise Mpamah and Tatiana Trubnikova contributed to the field and laboratory work. Christina Biasi and Jukka Juutilainen contributed to the design of the study, data analysis and writing. Pertti Martikainen contributed to study design and writing. Anne Kasurinen contributed to data analysis and writing. Markku Oinonen contributed to analysis of ¹⁴C samples and interpreting the ¹⁴C results.

II) Soroush Majlesi contributed to the field work, performed the data analysis, and wrote the draft of the manuscript. Jarkko Akkanen, Tiina S. Tuovinen and Jouni Sorvari contributed to study design, field work and writing. Jukka Juutilainen and Jonne Naarala contributed to study design and writing. Päivi Roivainen contributed to writing.

III) Soroush Majlesi contributed to planning the experiments, field and laboratory work, performed the data analysis and wrote the draft of the manuscript. Victor Carrasco-Navarro contributed to the laboratory work and writing. Jouni Sorvari contributed to study design, laboratory work, data analysis and writing. Sara Panzuto contributed to laboratory work. Jonne Naarala contributed to study design and writing. Jarkko Akkanen contributed to study design, field work and writing. Jukka Juutilainen contributed to study design, data analysis and writing.

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1 INTRODUCTION TO ENVIRONMENTAL RADIOACTIVITY AND POSSIBLE ADVERSE EFFECTS ON WILDLIFE

1.1 ENVIRONMENTAL RADIOACTIVITY

Radioactivity is defined as decay of radioactive material, containing unstable atomic nuclei that emit ionizing radiation to reach their stable forms (Chaturvedi and Jain, 2019; Nyhan et al. 2019). The unit of radioactivity is known as Becquerel (Bq), which corresponds to the quantity of radioactive material in which one nucleus decays per second (AMAP, 1998). The main forms of ionizing radiation emitted from radioactive isotopes of elements (radionuclides) are alpha particles, beta particles and gamma rays. Alpha particles are charged helium nuclei and highly ionizing with low penetration power. Beta particles are charged electrons that are moderately ionizing and have moderate penetration power, while gamma rays are photons (electromagnetic radiation), having the lowest ionizing and the highest penetration power (Bowlt, 1994). The adverse effects caused by radioactivity are related to the dose of radiation absorbed in tissues (Bowlt, 1994;

AMAP, 1998). The unit of absorbed dose is gray (Gy), which is defined as the amount of energy absorbed per unit mass (Jkg^-1), (Wahl, 2010; Piciu, 2017). The equivalent dose is commonly used to describe the probability of biological effects of ionizing radiation. It is derived from the physical absorbed dose by multiplying with a weighting factor that depends on the type and energy of the radiation (Piciu, 2017). The unit is sievert (Sv) in the SI system.

Radioactivity is often categorized into natural and artificial radioactivity. Natural radioactivity derives from decay of nuclei in the Earth’s crust and bombardment of the Earth by cosmic radiation, resulting in formation of natural radionuclides (Wahl, 2010; Cinelli et al. 2017; Sangiorgi et al. 2019). They are divided into long- lived primordial radionuclides (⁴⁰K, ²³⁸U, ²³²Th and ²³⁵U), decay chain radionuclides, which are formed due to the decay of primordial nuclides (radionuclides in the uranium, thorium and actinium decay series) and cosmogenic radionuclides that are formed continuously by interaction of high energy cosmic rays in the atmosphere (³H, ⁷Be, ¹⁴C, ²²Na), (Bowlt, 1994; AMAP, 1998). Artificial (man-made) radioactivity was formed since 1945 due to the nuclear weapon testing, military purposes, and nuclear plant waste (in forms of liquid and atmospheric emissions), followed by accidents such as Chernobyl and Fukushima in 1986 and 2011 respectively (Sangiorgi et al. 2019; Paatero and Salminen-Paatero, 2020).

Footprints of those activities are still detectable around the world.

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Research on environmental radioactivity has gained a lot of attention over the past years due to the global atmospheric fallout such as nuclear explosion and weapon testing, mining operations and use of nuclear energy. Nuclear power industries have become an important source of energy for many countries. In Finland, there are currently two nuclear power plants (Olkiluoto and Loviisa), providing about 30% of electricity demand (World Nuclear Association 2020). Hence, it requires well-planned provisions and management of radioactive waste, to avoid possible release of radionuclides due to poor planning and construction of waste repositories. Currently, the deep geological disposal of radioactive waste is considered as the best method for management of long-lived radionuclides (IAEA, 2009a; Posiva, 2016). In Finland, deep geological disposal facilities are being built and the repository is developed according to the KBS-3 concept. In this method radioactive waste is sealed in water- and gas-tight copper canisters and isolated in a geological repository, constructed in the bedrock at the minimum depth of 400 m.

The design is based on multiple supportive, yet independent barriers that guarantee the overall functioning of the system and safety of the environment in the long-term (Posiva, 2012).

Another source of environmental radioactivity is mining activities. Mining operations have become globally important since they are the basis to supply nuclear fuel in nuclear reactors. Uranium mining operations were significant in Finland until 1990s (AMAP, 2009). Small-scale operations were mostly implemented in eastern Finland (Paukkajanvaara) and southern Finland (Askola), (Colpaert, 2006; AMAP, 2009; Tuovinen et al. 2016). Uranium exploration started in Finland again mainly in Northern Karelia and Lapland in 2004 due to the global demand (AMAP, 2009). The major sources of contamination from mining operations are waste rock piles and mill tailings, from which radionuclides can leach and thus be incorporated in terrestrial and aquatic ecosystems (Tuovinen et al. 2016).

1.2 RADIOECOLOGY

Radioecology is the study of the behavior of naturally occurring and artificially produced radionuclides in the biosphere. This discipline investigates the risks of adverse effects from radioactive pollutants to humans and non-human biota.

Radionuclides released into the biosphere can be incorporated into different environmental compartments such as soil, water, plants and air, and subsequently enter the food chain. The most common terrestrial pathway for humans is the soil- plant-animal-human pathway via milk or meat, while fish, possibly exposed to contaminated water/sediment is a widely consumed aquatic resource (AMAP, 1998).

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2016). Distribution coefficients are used to predict the concentrations and dispersion of radionuclides between aqueous and solid phase as the ratio of radionuclide concentration in soil or sediment to the concentration in water or soil solution (IAEA, 2004). Models suitable for equilibrium conditions are often used for e.g., assessing risks related to geological disposals, where equilibrium conditions can be assumed because of the slow release of radionuclides. In unexpected accidental releases of radionuclides, dynamic approaches are more practical as CR can under- or over-estimate the exposure. Such approaches are based on uptake and turnover processes by first-order kinetics (e.g., ingestion, sorption, and biochemical behavior of organisms) in which biota- and element-specific data on biological half-lives are necessary (Beresford et al. 2015). Radioecological assessment models are continuously developing for aquatic and terrestrial environments (IAEA, 2017) to better represent theoretical and empirical understanding of transfer of elements into organisms. Such development has enabled more accurate radioecological analyses for exposure to radiation (Beresford et al. 2015; IAEA, 2017). However, transfer of elements into organisms is site- specific and ecological factors such as seasonal variation and ecological sensitivity as well as biological complexities need to be considered (AMAP, 2004; Väänänen et al. 2018). Current models are mostly developed from temperate environments and less radioecological data is available on boreal ecosystems, which is necessary to calibrate the models for these northern ecosystems. Boreal ecosystems are characterized by relatively low temperatures and short growing seasons. Therefore, more information on such ecosystems is needed.

1.3 ELEMENTS RELEVANT TO RADIOACTIVE WASTE

1.3.1 Uranium (U)

Naturally, uranium exists in oxidation state in forms of U⁶⁺ or U⁴⁺ (Abdelouas, 2006;

IRSN, 2012). Under oxidizing conditions, U⁶⁺ is present as uranyl ion (UO22+), which is dominantly acidic and highly soluble in water (Driver, 1994; Wall and Krumholz, 2006). Excessive acidic conditions originated from mill tailings increase the mobility of radionuclides and other toxic metals and thus negatively impact the ecosystem and organisms (Gao et al. 2019). In forms of carbonate complexes ([UO2(CO3)²]^2- and [UO2(CO3)3]⁴), it is even more mobile under neutral to alkaline conditions (Abdelouas, 2006). Nevertheless, under reducing conditions, U⁴⁺ is present as UO2

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phase, which is highly insoluble in water. Uranium is mostly found in rocks and uranium ores and in small amounts in soil and water (Peterson et al. 2007; Wang et al. 2019). When released to the soil as a result of rock breakdown, it can end up into streams, lakes and surface water via wind advection and water movement.

Uranium has three major radioactive isotopes, of which ²³⁸U is the most abundant isotope (99.2%), while less than a percent (0.72%) of natural uranium is ²³⁵U (Gao et al. 2019). The fraction of ²³⁴U in natural uranium is very small (0.0057%) but is more radioactive than the other isotopes. Uranium is mainly an alpha emitter and weakly radioactive, with very long half-lives from 244000 years for ²³⁴U to 5 billion years for ²³⁸U. Other sources of uranium are mining operations, waste from the nuclear fuel cycle, military use, use of coal and phosphate fertilizers which are rich in ²³⁸U (IRSN, 2012; Liesch et al. 2015). The importance of this element stems from its presence and persistence throughout the nature. It is both chemo- and radiotoxic and known as a long-lived parent nuclide of dose-contributing daughters such as

210Po and ²²⁶Ra. It is widely used as fuel for nuclear reactors. Radiological toxicity is dominated by internal exposure to ²³⁵U, which is depleted for military use and enriched for nuclear power reactors (as the main fissile isotope of uranium).

However, it is noteworthy that ²³⁸U (because of its abundance) has the greatest biological effects on mammals, targeting kidney, bone, and other organs in animals (Simon et al. 2018; Gao et al. 2019; Wang et al. 2019). Data on radiotoxicity of uranium is insufficient and further research on this topic is required.

1.3.2 Radiocarbon (¹⁴C)

Radiocarbon (¹⁴C) is one of the important radionuclides with relatively long half- life (5730 years). It is a β emitter with extremely small natural abundance (one part per trillion). Natural ¹⁴C forms when cosmic radiation converts nitrogen in the upper atmosphere into radiocarbon (Major, 1993; Peterson et al. 2007; IRSN, 2010).

This naturally occurring radiocarbon reacts with oxygen to form carbon dioxide (Major, 1993). Two major chemical forms of ¹⁴C are ¹⁴CO2 (mineral) and ¹⁴CH4 (organic), (IRSN, 2010). Carbon dioxide enters the biosphere mainly through uptake of plants via photosynthesis and then being transferred further in the food chain by animals that consume plants.

Artificial sources of ¹⁴C are releases from nuclear wastes from reactors and repositories, global fallout, and other sources such as medical, industrial and research (IRSN, 2010). Most of ¹⁴C in nuclear reactors is generated from the reactions occurring in the fuel (IRSN, 2010). The gaseous effluents of boiling water reactors are mostly ¹⁴CO2 (95%), while in pressurized water reactors are mainly in organic form (e.g. ¹⁴CH⁴ with 80%) and to less extent (20%) in form of ¹⁴CO² (IRSN, 2010). From

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23 deep geological repositories, ¹⁴C can be released due to corrosion of metals (Heiko- la, 2014) and decomposition of organic materials, in forms of both dissolved and gaseous species (¹⁴CO2, ¹⁴CH4, or low molecular weight organic compounds), (Mazeika, 2010; Mobbs et al. 2013, 2014; Doulgeris et al. 2015). Nuclear explosions can also emit radiation (neutrons) that interacts with atmospheric nitrogen to create

14C (IRSN, 2010). The estimated release of ¹⁴C from such explosions was 3.5 x 10¹⁷ Bq before 1972, and it increased by 1% due to later explosions (UNSCEAR, 2008).

The importance of this radioisotope is its incorporation with stable isotopes of C, which are essential to living organisms. ¹⁴C mixed with other C isotopes is readily transferred to animals and plants and has great potential for incorporation into cellular components due to its long half-life. Therefore, even though the radiotoxicity of ¹⁴C is relatively low, the radioecological concern is high because it is actively metabolized into the organisms.

1.3.3 Other important elements

According to the Posiva report (2010), there are certain radionuclides that are important for long-term safety assessment of radioactive waste in terms of their release from different sources such as waste repositories and mining operations.

There are 11 key radionuclides for biosphere assessment, and three of them are ranked as top priority radionuclides (¹⁴C, ³⁶Cl and ¹²⁹I), because they dominate the dose in the biosphere calculation in realistic situations. The high priority radionuclides ⁹³Mo, ⁹⁴Nb, ¹³⁵Cs, ⁵⁹Ni, ⁷⁹Se, ⁹⁰Sr, ¹⁰⁷Pd and ¹²⁶Sn contribute significantly to doses in some biosphere prediction models (Posiva, 2010). According to the Swe- dish nuclear fuel and waste management Co. (SKB), the elements in which their radionuclides are considered for biosphere safety assessment of high-level waste are C, Cl, I, Cs, Mo, Ni, Nb, Ra, Se, Sr, Tc, Th and U (Kautsky et al. 2015). In addition to these elements, some other radionuclides such as ⁴¹Ca, ²³¹Pa, ²²⁷Ac, ²³⁹Pu and

99Tc were also considered for transport modelling of low- and intermediate-level waste by SKB (Kautsky et al. 2016). Overall, the list is very similar to radionuclides suggested by Posiva (2010). In this section, the elements, relevant to radioactive waste, which are investigated in this work are specifically described below. They are important for ecological risk assessment of ionizing radiation in boreal environments due to mining operations and nuclear power plants.

Chlorine is known as essential element for life and usually bound to other elements such as sodium. It can be found in salt deposits, crustal rocks, and seawater (Peter- son et al. 2007). Among the radioactive isotopes of Cl, only ³⁶Cl is important for safety assessments because of its long half-life of 300000 years, emission of beta particles and high mobility in the environment. It is highly reactive and has a great

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potential to be absorbed to any biological tissues after ingestion or inhalation. It is naturally generated by cosmic radiation from atmospheric argon (Sinclair and Ma- nuel, 1974; Petrov and Pokhitonov, 2020, Svensson et al. 2021). The key sources of

36Cl are radioactive waste from the nuclear fuel cycle and atmospheric deposition during nuclear weapon tests between 1952 and 1958 (Peterson et al. 2007, Svensson et al. 2021). Furthermore, ³⁶Cl is widely present in materials used in nuclear reactors and as such will be present in radioactive wastes (Petrov and Pokhitonov, 2020).

Cobalt is another essential element mostly associated with sediment and suspended particles in water and chemically bound to other elements such as Ni (Fisher, 2011).

Among its radionuclides, ⁶⁰Co decays with relatively long half-life of 5.3 years and emits high energy gamma rays. Major sources of ⁶⁰Co are wastes from the nuclear fuel cycle and medical wastes used in scanning equipment (Peterson et al. 2007).

60Co is also used in wide range of applications, including medical purposes (DeCar- lo and Matthews, 2019).

Molybdenum is metallic element with very strong hardness at high temperature, mainly used as sheathing of enriched nuclear fuels (Barceloux and Barceloux, 1999;

IRSN, 2003). The common radioisotope of molybdenum is ⁹⁹Mo which is a beta emitter with a half-life of 66 hours. Molybdenum is a rare metal which is naturally found in earth’s crust (0.001%). Radioactive waste from nuclear fuel reprocessing plants and atomic weapon testing are the major sources of radioactive isotopes of molybdenum (IRSN, 2003). Molybdenum is an essential element for animals, plants, and microorganisms. It is highly associated with copper and sulfur (No- votny and Peterson, 2018). High intake of molybdenum inhibits the absorption of copper, resulting in anemia, gastrointestinal disturbances, and growth retardation (Novotny and Peterson, 2018). Radioactive isotopes of molybdenum are of artificial origin (products of fission), being continuously released in the environment and thus categorized as an important element for safety assessment.

Nickel is a silvery-white metal that is found in various ores in nature and to less extent in soil (Peterson et al. 2007; Poonkothai and Vijayavathi, 2012). Two important radioactive isotopes of nickel are ⁵⁹Ni and ⁶³Ni, which decay with half-life of 75000 years by electron capture and 96 years by emitting beta particles, respectively. They originate from reprocessing of spent nuclear fuel and to some extent from atmospheric fallout (Peterson et al. 2007). Exposure to radioactive isotopes of nickel via ingestion or inhalation may increase the likelihood of cancer.

Selenium is naturally found in rocks, water, and soil especially in soils near volca- noes (Peterson et al. 2007). Selenium is an essential element (metalloid) and chemical analogue of sulfur, which exists in forms of gray crystal and red powder (IRSN, 2005a; Peterson et al. 2007; Reich and Hondal, 2016). However, depending on its

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25 concentration it can be toxic to animals (Avery and Hoffmann, 2018; Vinceti et al.

2018). According to U.S. Department of Energy (DOE), ⁷⁹Se is the most important radioactive isotope of selenium with a long half-life of 650000 years, emitting beta particles. It is present in spent nuclear fuel and wastes, generated from reprocessing the fuels (Peterson et al. 2007; Pisarek et al. 2021; Savoye et al. 2021). Because of

79Se’s long half-life and possible release as radioactive waste, it is considered as an important radionuclide for risk assessment.

Strontium is an alkaline soft metal that can be found in silver and grey colors in sandstones and carbonate rocks (IRSN, 2005b; Peterson et al. 2007). It is strongly bound to soil organic matter and could be taken up into animal bones due to bioge- ochemical similarity to calcium (Ca) (Burger and Lichtscheidl, 2019; Snoeck et al.

2020). The major radionuclide of strontium is ⁹⁰Sr with a long half-life (29 years); it decays to ⁹⁰Y by emitting beta particles (Burger and Lichtscheidl, 2019). ⁹⁰Y emits extra beta particles to decay to ⁹⁰Zr (Burger and Lichtscheidl, 2019). ⁹⁰Sr is a fission product generated in nuclear plants as well as fuel reprocessing (IRSN, 2005b; Pe- terson et al. 2007; Burger and Lichtscheidl, 2019). Moreover, it is vastly available in soil particles, resulting from past global fallout. However, due to its relatively high mobility it can also be transported to groundwater (Peterson et al. 2007).

Zinc is an essential element for all living organisms and is very common in earth’s crust (Broadley et al. 2007, Kabata-Pendias, 2011). Therefore, it is constantly taken up by animals and plants. Zinc can be naturally found in air, soil, and water, or because of human activities by production of steel, burning of coal and zinc fertilizers on agricultural soil (Peterson et al. 2007). In aquatic environments zinc is dissolved or suspended (as fine particles) in water or associated with particles in the bottom (Peterson et al. 2007). In terrestrial ecosystems, it is bound to particles in the upper layers of soil but depending on physico-chemical properties of the soil it can also leach into the groundwater (Peterson et al. 2007). The long-lived radioactive isotope of zinc is ⁶⁵Zn with a half-life of 244 days, decaying by electron capture. The key source of this radionuclide in the environment is nuclear weapon testing and atmospheric fallout (Win and Masum, 2006). Due to availability of ⁶⁵Zn during the second world war and importance of zinc absorption for all living organisms, this radionuclide has become important. Since it can be readily taken up by organisms if possibly released from waste repository and other sources, it has been considered as one of the important radionuclides in safety assessment of radioactive waste.

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1.4 TRANSFER OF RADIONUCLIDES TO ORGANISMS

Release of radionuclides into ecosystems can be in forms of low molecular mass (LMM) ions, complexes, colloids, or particles (Salbu and Lind, 2020). These forms affect the bioavailability and uptake in living organisms. For example, LMM ions, colloids and nanoparticles tend to be more mobile and bioavailable, while particles hinder the transfer (Salbu, 2009). The speciation of radionuclides also changes with time due to interactions with soil/sediment particles, which delays the mobilization.

However, in presence of acidic LMM ions, radionuclides can remobilize and form complexes with other elements or contaminants and become available (Salbu, 2009).

Such complexes may act synergistically or antagonistically in the process of uptake.

Apart from the speciation of radionuclides, characteristics of ecosystems and organisms influence the transfer of radionuclides into non-human biota.

1.4.1 Transfer of radionuclides in aquatic ecosystem

Freshwater ecosystems cover about 1% of the earth’s surface but are considered as the habitat for over 10% of all animal species and 35% of all vertebrate species (Stendera et al. 2012). Release and further mobilization of radioactive waste from repositories and mining operations could have negative effects on freshwater bodies. Therefore, risk assessment of ionizing radiation in such ecosystems is essential.

A concentration ratio is commonly used to predict the transfer of elements into organisms. Although the mechanism of uptake in the aquatic environment is very complex, data on transfer of radionuclides in boreal freshwaters based on concentration ratio is still needed. This approach has been widely used in previous studies and CR values in freshwater ecosystems have been reported by IAEA (2010, 2014).

The reported CR values in aquatic biota are predicted from water and sediment as possible sources of uptake. However, the need for development of process-based modelling have been emphasized in other studies, reporting that transfer of radionuclides into biota may also depend upon other environmental parameters (Salbu, 2009; Hinton et al. 2013; Konovalenko et al. 2017; Almahayni and Houska 2020). In general, uptake of radionuclides depends on sources, deposition, radionuclide speciation, mobilization, and aquatic organisms as well as physico-chemical properties of the water and sediment of receiving ecosystems (Skipperud and Salbu 2018;

Väänänen et al. 2018).

Once radionuclides disperse in the freshwater environment they can be incorporated into the water or absorbed by solid particles (IAEA, 2009b, 2010). Dissolved radionuclides in water can also be absorbed by sediment particles at the bottom of lakes, transferred to deeper layers and/or be taken up by organisms at the benthic

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27 level (IAEA, 2009b, 2010). Benthic organisms are subsequently hunted by fish and other large animals at higher trophic levels. On the other hand, elements absorbed to solid particles can also remobilize in the water by bioturbation or diffusion, in- teracting with suspended matter and to then be taken up by other species at a higher level (IAEA, 2009b, 2010). The concentration of radionuclides in the water column is also attributed to changes in pH and dissolved oxygen content of water/sediment in which increase in the latter can increase the redox potential and mobility of redox active species associated with sediment (Geng et al. 2019).

In general, the bioavailability of elements in water is highly related to water chemistry such as hardness, salinity, ligand complexes and pH (Väänänen et al. 2018).

External environmental factors such as seasonal variation and changes in oxygen and temperature are also important especially in the boreal zone, where such changes are huge (Väänänen et al. 2016). In the presence of high concentrations of oxygen in water, some elements become more bioavailable due to mobility and oxidation of metal-binding sulfide to sulfate (Di Toro et al. 1992; De Jonge et al.

2012a), resulting in changes in acid-volatile sulfides (AVS) and accumulation of elements in benthic feeders (De Jonge et al. 2012b). Furthermore, it can also enhance mobility and leaching of sediment-bound metals to water column (De Jonge et al.

2012a). In sediment, however, bioavailability is mainly controlled by competition of cations for binding to organic matter, solubility, ion exchange potential and capabil- ity to bound to Fe-Mn oxides (Väänänen et al. 2018).

It should be also noted that bioaccumulation of elements depends on organism characteristics, which are attributed to feeding habits, age, size, position in the food chain and tolerance of organisms (e.g., gut passage time and gut chemistry) to certain elements (Simpson and Batley, 2007; IAEA, 2010; Carvalho, 2018). According to the IAEA (2010), uptake of elements into fish is best described with radionuclide concentration in water, while for benthic dwellers and deposit feeders, sediment plays a crucial role as well.

Among aquatic plants, studies have shown that the uptake of radionuclides is mostly affected by species characteristics and environmental parameters. For in- stance, in a study carried out by Jha et al. (2016) in freshwater ecosystems near uranium mill tailings, a broad range of CR values were observed for different plants.

The results of this study indicated that the U concentration in filamentous algae is correlated to water, whereas the concentration of uranium is correlated to sediment in sediment-rooted plants. Furthermore, a significant correlation was found between the U concentration and Mn, Fe and Ni concentration for free-floating plants and sediment-rooted plants. In other studies, accumulation of radionuclides in aquatic plants is reported to be attributable to seasonal patterns, plant characteristics, amount of biomass, exposure to sunlight, pH, and concentration of radionu-

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clides (Saleh, 2012; Saleh et al. 2017; Ganzha et al. 2020). Saleh (2012) reported that uptake of radiocesium (¹³⁷Cs) in a floating plant, water hyacinth (Eichhornia cras- sipes) is adversely correlated with activity concentration and directly proportionate to plant biomass, presence of ⁶⁰Co and sunlight, while uptake of ⁶⁰Co was dimin- ished by the presence of ¹³⁷Cs. Moreover, in the study by Saleh et al. (2017), high uptake of ⁶⁰Co and ¹³⁷Cs was observed (95% and 65% respectively) by Ludwigia stolonifera, in which pH had less impact on uptake compared to other variables (e.g., activity of radionuclides, plant masses or lighting). An elevated rate of uptake of

90Sr and ¹³⁷Cs was also observed during vegetation growth period in 10 species of higher aquatic plants in Glyboke Lake, Chernobyl (Ganzha et al. 2020).

The transfer of radionuclides into living organisms is very site-specific and less data on boreal ecosystems is available compared to other environments. For example, previous studies on boreal forests questioned the linear uptake of radionuclides into plants and animals (Roivainen, 2011; Tuovinen, 2016). Huge variation in bioaccumulation of radionuclides was also observed within Canadian aquatic ecosystems, showing under- or over-prediction of radiological risks based on bioaccumulation factor as the only parameter (Brinkmann and Rowan, 2018). A similar approach based on site-specific results rather than generic values has been also recommended by Monte et al. (2009). It has been reported that physico-chemical properties and physical processes such as water current, dispersion caused by turbulent motion of water, sedimentology, and resuspension of radionuclides from sediment play a major role in transfer of radionuclides in aquatic ecosystems (Monte et al.

2004, 2009). Such fluxes determine the transfer of radionuclides from water to sediment or vice-versa.

In general, the process of uptake in aquatic ecosystems involves very complex hy- drological, physical, and geological phenomena, which has been a major challenge for radioecologists to present accurate prediction of radionuclide transfer into organisms. Hence, further research is needed to develop current models in boreal aquatic ecosystems.

1.4.2 Transfer of radionuclides in terrestrial ecosystem

Similar to aquatic ecosystems, transfer of radionuclides in soil and terrestrial ecosystems depends on numerous variables and is often described by the K^d concept between solid phase and soil solution. Higher Kd values indicate sorption of radionuclides in the solid phase, which increases the residence time in soil, while lower values indicate mobility of radionuclides in soil solution and possible leaching to deeper soil layers and groundwater (IAEA, 2010). The mobility of radionuclides is generally controlled by convection velocities, diffusion, radionuclide speciation and

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29 soil physicochemical properties (cation exchange capacity, pH, organic matter, and clay content), (IAEA, 2010). In addition to soil parameters, climatic condition, time, and species differences influence the uptake (Golmakani et al. 2008). For example, accumulation of radionuclides among plant species from the same soil might mas- sively differ (Anspaugh et al. 2002; Golmakani et al. 2008). Variabilities in plants include metabolic and biochemical mechanisms of uptake, detoxification mechanism and plant available concentration in rhizosphere (IAEA, 2010). Therefore, using CR values as the only tool to predict the uptake of radionuclides in terrestrial organisms may not be accurate (Ehlken and Kirchner 2002). In general, soil frac- tions with heavy clay and organic matter content tend to have higher cation exchange capacity (CEC) by holding cations due to more negative charges on soil surface, while sandy soils with less clay content have fewer positions to hold cations (Ketterings et al. 2007; Saidi, 2012; Keck et al. 2017). Many radionuclides, such as Cs and Sr, act as chemical analogues of essential nutrients like Ca²⁺ and K⁺respectively, which can be taken up by plants via ion exchange reactions occurring in soil (Ehlken and Kirchner 2002). However, in the presence of hydrogen ions and increase in soil acidity (low pH), the competition with other cations for binding to soil particles increases, resulting in release of radionuclides (e.g., uranium) in soil solution that can be taken up by plants via root uptake (Greger, 2004; Ketterings et al. 2007; IAEA, 2010). Furthermore, soil microorganisms have a potential role in migration and cycling of radionuclides in the solid/solution interface by uptake of radionuclides, changing soil structure and altering soil pH via organic matter production, which may also act as ligands for radionuclides (Tamponnet et al. 2008;

IAEA, 2010). In soil animals, several factors as described earlier in this section (pH, DOC, CEC) are significant for assessment of bioavailability. In addition, physiology and morphology of animals, diet, retention time of radionuclides in the animals’

bodies, biotic ligand sites and bioaccumulation mechanisms are involved in the process of uptake (Bocock, 1981; Ardestani et al. 2014).

These variables and large variation in CR values of flora and fauna of boreal forests are widely discussed in previous studies, carried out in the field and laboratory by Roivainen (2011) and Tuovinen (2016). Therefore, the need for further development of radioecological models and accurate prediction of radionuclide transfer based on chemical, physical and biological processes has been emphasized in terrestrial ecosystems.

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1.4.3 Behavior and transfer of radiocarbon (¹⁴C) in the biosphere

The transfer of ¹⁴C into plants and animals is different from that of other radionuclides, which is often described by CRs. The transfer of ¹⁴C is thus reviewed here separately. ¹⁴C released from nuclear facilities and radioactive waste repositories mixes with stable isotopes of C (¹²C and ¹³C) and is taken up by organisms like other isotopes of C. Its long half-life (5730 years) also increases the radioecological concern once entered in the food chain. Moreover, ¹⁴C can also distribute in gaseous form (e.g., CO², CH⁴) in the atmosphere at the global scale (Pérez-Sánchez et al.

2009).

Once ¹⁴C is released from spent nuclear fuel or deep geological disposal, e.g., in accidents or unexpected scenarios, it can be actively taken up into the biosphere by animals and plants (SKB, 2019). Organisms take up ¹⁴C either by fixation of atmospheric CO2 by plants (Pérez-Sánchez et al. 2009; IRSN, 2010; Mobbs et al. 2014;

Limer et al. 2017) or assimilation of CH⁴ by soil methanotrophs (through microbial decomposition of organic matter) and incorporation into the ‘’brown’’ food chain (Serrano-Silva et al. 2014; Knief, 2015). The importance of brown food web has been discussed in several studies (Soininen et al. 2015; Zou et al. 2016; Cordone et al.

2020). This food web is based on consumption and decomposing of organic matter by detritivores, which results in release of nutrients in terrestrial and aquatic systems. In terrestrial ecosystems, plants mainly take up atmospheric ¹⁴CO2, which is consequently consumed by herbivorous animals in the food chain. However, ¹⁴C incorporated in the soil can be either directly taken up via roots or indirectly re- assimilated as soil-derived ¹⁴CO2 by soil respiration. Transfer of soil-derived C has been investigated in few studies (Table 1). In general, the root uptake is known as a minor pathway, ranging from 1% to 3% (Yim and Caron, 2006; Van Dorp and Brennwald 2009; Mobbs et al. 2014; Li et al. 2018). Re-assimilation of soil-derived CO2 by plants photosynthesis has been rarely studied. The rate of re-assimilation in plant canopy is assumed to be a few percent (Mobbs et al. 2014). ¹⁴C released from the soil system may also dissolve in soil water. Once dissolved in soil solution, it can end up into plants (via roots) in form of carbonate ions (Garnier-Laplace and Roussel-Depet 2010). The assimilation of ¹⁴C from soil solution into plants might also occur passively through decomposition of contaminated organic carbon and potential re-assimilation of ¹⁴CO2 by leaves through photosynthesis (Mobbs et al.

2014). Some of these assimilated C is leached into the soil through root exudation and thus increase the C storage (Lange et al. 2015). The transport of ¹⁴C to deeper layers is controlled by the movement, velocity, and direction of groundwater flow.

During the process of transport, other physical processes such as precipitation, sorption and diffusion will impact the rate of transport (Pérez-Sánchez et al. 2009).

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31 The ¹⁴C taken up by organisms can also re-enter the soil or aquatic system (soil solution or groundwater) in organic form as plant litter and leftovers of soil animals and microorganisms.

The amount of C uptake from soil and transfer into plants is attributed to numerous factors such as soil physicochemical properties and plant species. In general, C in soil organic matter accumulates gradually and thus due to the longer turnover rate it remains old in soil compared to atmospheric C (Ontl and Schulte, 2012; Gross and Harrison, 2019). Another important pathway for transfer of ¹⁴C from soil to plants is methanotrophy. Currently it is cautiously assumed in the long-term safety assessments that all ¹⁴CH⁴ is oxidized to ¹⁴CO² via methanotrophs to enter the food chain through plant uptake (Humphreys et al. 2011). Decomposition of methane by methane-oxidizing bacteria (methanotrophs) is one of fundamental means of soil C transfer to plants and soil animals. The rate of methanotrophy is highly related to species and activity mechanisms of microorganisms and their quantity at different soil depths and climate (Hanson and Hanson, 1996; Murrell, 2010). In northern drained peatlands, most of the produced methane is reported to be consumed before emitted to the atmosphere, thus being available from soil to plants especially in oxygen-rich environments (Mobbs et al. 2014). The assumption that all ¹⁴CH⁴ is oxidized to ¹⁴CO2, however, may not be true for natural peatlands or wetland aeras where high CH4 emissions are usually reported (Abdalla et al. 2016; Wen et al.

2018), thus emphasizing the need for ecosystem-specific data.

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Table 1. Transfer of soil C into plants

Study Methods Transfer of soil C into

plants

Ford et al.

2007

13C labelling; contribution of soil C was determined based on excess of ¹³C in seedlings relative to mean signal of seedlings in unla- beled treatment

1.6% root uptake for pine seedling

Tagami et al.

2009

Estimation of transfer from soil to plants by using stable isotopic ratios (¹³C/¹²C)

root uptake for rice up to 1.6%

Tagami and Uchida, 2010

Estimation of transfer from soil to plants by using stable isotopic ratios (¹³C/¹²C)

0.6% root uptake for rice and up to 7.3% for other crops

Li et al. 2018

Radiolabeling of soil samples with

14C-Carbamazepine and measurement of ¹⁴C activity in plants

maximum ¹⁴C-

Carbamazepine uptake of 2.19%, 2.86% and 0.25%

was found from soil in celery (stem vegetable), carrot (root vegetable) and pak choi (leafy vegetable).

Nie et al. 2020

Radiolabeling of soil samples with

14C-triclosen and measurement of radioactivity of plant samples

1.02% root uptake of ¹⁴C- triclosan from soil to pea- nut plants

In aquatic systems, CO2 is exchanged between water bodies and the atmosphere via uptake of atmospheric C by phytoplankton and aquatic plants as dissolved inorganic carbon (DIC), mainly in forms of carbonate and bicarbonate (IRSN, 2010;

Rasilo, 2013; Limer et al. 2017; SKB, 2019). Methanogens will also use dissolved organic matter, derived from autochthonous and allochthonous origin to form methane (CH4) under anoxic condition. The methane is subsequently oxidized by methane-oxidizing bacteria (MOB) to form CO² in presence of oxygen, used as source of energy for aquatic animals at higher trophic level (Sanseverino et al. 2012). The release of terrestrial organic matter into aquatic systems through soil solution and sedimentation may end up transferring C into deposited sediment and organic matter, which are sources of food for many benthic species (Major, 1993). Transfer of organic C (up to 30%) from sediment and terrigenous peat has been detected in benthic animals (Chironomus sp. and Lumbriculus variegatus) under controlled laboratory environment (Pham, 2020).

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1.5 EFFECTS AND TOXICITY OF ELEMENTS, RELEVANT TO RADIOACTIVE WASTE ON WILDLIFE AND ECOSYSTEMS

Traditionally, the key focus of possible adverse effects of radioactivity has been on human health and according to the International Commission on Radiological Pro- tection (ICRP, 1977), the protection of humans from radiation would likely be suffi- cient for protection of wildlife. However, in recent years the focus has shifted to a new paradigm for protection of wildlife, and it has been suggested that wildlife populations should have their own endpoints (Dallas et al. 2012; Bradshaw et al.

2014; Caffrey et al. 2014; Adam-Guillermin et al. 2018; Beresford et al. 2020; Haanes et al. 2020; Johnson et al. 2020). The mechanisms of uptake of radionuclides into non-human biota and their impacts at ecosystem level may be different from effects on humans. It has been suggested that, rather than studying effects on single species, the impacts of ionizing radiation should be investigated based on interaction of several species at community and ecosystem levels, including high ecological complexity and environmentally relevant doses (Haanes et al. 2020).

1.5.1 Uranium (U)

Uranium is both chemo- and radiotoxic. According to the environmental quality standard in France, the predicted no effect U concentration of freshwater (PNEC

freshwater) is 0.3 µg L^-1. At high levels, the toxicity is dominated by uranyl ion under oxic conditions in freshwater animals (IRSN, 2012; Crawford et al. 2018). It is highly bound to solid phases and forms complexes with phosphate and sulfate ions, which may enhance its accumulation in sediment, particularly under acidic conditions (Crawford et al. 2018). The incorporation of uranyl ions with DOC can also increase the solubility and thus bioavailability of U in aquatic organisms (Crawford et al.

2018).

The PNEC values vary to huge extent from 0.3 to 3510 µg L^-1due to uranium speciation and different water physicochemical properties (IRSN, 2012). PNEC for radiotoxicity of ²³⁸U for freshwater environment was suggested to be protective at 3.2 µg L^-1by Mathews et al. (2009). In contaminated freshwaters, the concentration of U has been reported to range from 12 µg L^-1to 2 mg L^-1(Simon et al. 2013).In general, uranium targets organs such as kidney and bones. In kidneys, U is normally filtered through renal glomerulus in soluble form, while replacement of calcium with uranium in the hydroxyapatite traps uranium in bones, depending on physiology of organisms (vertebrates vs invertebrates), (IRSN, 2012). It is reported that chemical toxicity of uranium is ameliorated by increasing water hardness, alkalinity, and

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concentration of dissolved organic matter (DOM). U toxicity is also species depend- ent, which could vary under different circumstances. For example, several symptoms such as increase in respiratory ventilation, swimming difficulties, malfunc- tioning of gills and fins and DNA damage have been reported in fish due to U toxicity (Bourrachot et al. 2014; Annamalai and Arunachalam, 2017). Importantly, decrease in reproduction has been reported to be a major endpoint in roach and zebrafish, with effects on their reproduction cycle and the protein content of ovaries after chronic exposure (Frelon et al. 2020). Concerning radiotoxicity, of ²³⁸U, alpha particles have been reported to cause DNA damage in fish cells (IRSN, 2012). Toxic effects of U on benthic organisms have also been reported, indicating impacts on larval development and delay in time to emergence in chironomid species (Musca- tello and Liber 2009) and effects on growth and fertility in Daphnia (Antunes et al.

2007). Liber et al. (2011) reported that the acute U toxicity in Hyalella azteca is best correlated with the U pore water concentration, with a 10-d LC50 of 2.15 mg L^-1. The no observed effect concentrations (NOECs) for growth of H. azteca and Chironomus dilutus were reported to be 0.67 and 0.21 mg L^-1respectively (Liber et al. 2011).

1.5.2 Radiocarbon (¹⁴C)

Radiocarbon emits beta particles, which have moderate penetration and ionizing power. Thus, its biological effects result mainly from internal irradiation (IRSN, 2012). The problem with ¹⁴C is that it has almost identical chemical characteristics with stable carbon isotopes, which are fundamental components of organic elements. Even though the radiotoxicity of ¹⁴C is relatively low, radioecological concern is high because ¹⁴C effectively participates in the metabolisms and is retained in the biological circulation. It also has a relatively long half-life. Thus, dose contri- butions from ¹⁴C have been demonstrated to be considerable in recent studies (Kryshev et al. 2020; Tsuyoshi et al. 2020). It has also been demonstrated that its incorporation into cellular components results in DNA damage, mutations, and cell death (Le Dizès-Maurel et al. 2009). In another study, exposure to 50 mg kg^-1 of ¹⁴C ameltolide in pregnant rats showed the highest concentration in maternal liver at 5.86% of dose at 5 h (Pohland and Vavrek, 1991). The maternal liver and kidney showed higher concentrations than maternal plasma concentrations at all time points. In another study, incorporation of radiocarbon, originated from nuclear weapon testing was detected in the growing teeth of beluga whale (Delphinapterus leucas), derived mostly from its prey rather than water (Stewart et al. 2006).

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35 1.5.3 Other elements

When ³⁶Cl is taken up into animal bodies, its beta and gamma radiation decrease organ and body weights due to incorporation in cellular components (Peterson et al. 2007). Other studies demonstrated toxicity of Cl in fish by growth inhibition in rainbow trout (Oncorhynchus mykiss), (Svecevičius et al. 2005) and decreasing tolerance of Pink salmon (Oncorhynchus gorbuscha) and Chinook salmon (Oncorhynchus tshawytscha) to residual Cl at high temperature (Stober and Hanson, 1974). Among other species, freshwater mussel (Limnoperna fortune) showed an increase in mortality rate because of Cl toxicity (Cataldo et al. 2003). Radiotoxicity of ⁶⁰Co is mostly related to its very high-energy gamma radiation (IRSN, 2001). Several other toxici- ties at the cellular level and DNA damage in aquatic species such as Hydra have been observed (Zeeshan et al. 2017). Molybdenum is another essential element, which induces toxicity in organisms, if taken excessively. Toxicity of Mo especially in cattle includes neurological disturbances, early death, and hair depigmentation (Anke et al. 2010). Poor growth, anemia and central nervous system degeneration have also been reported in rats, chickens, and rabbits (Pitt, 1976). Among soil organisms, survival of earthworms (Eisenia andrei), Collembola (Folsomia candida) and enchytraeids (Enchytraeus crypticus) was affected by Mo toxicity (IRSN, 2003; Van Gestel et al. 2011, 2012). Toxicity in aquatic animals largely varies among species.

Different symptoms such reprotoxicity in mussels, liver, and gastrointestinal effects in rainbow trout, after chronic exposure, and reduction in shell growth in oysters have been observed (Eisler, 1989). Concerning Ni, many effects in freshwater biota such as respiratory problems and an increase in oxidative stress and impacts on shells in molluscs have been observed (IRSN, 2002; Blewett and Leonard, 2017). At high concentrations, Se toxicity occurs as disruption in metabolism and enzymatic system, associated with cellular respiration (Koller and Exon 1986; Tinggi, 2003;

IRSN, 2005a). It mostly induces developmental and teratogenic toxicity (e.g. de- formed embryos, reproduction toxicity and mortality) in fish, frogs, and aquatic birds (Browne and Dumont 1979; Ohlendorf, 1989; Lemly, 1997; Hamilton, 2004). Sr has a relatively low toxicity, but due to its similarity to Ca, it can store in animals’

bones and cause neoplasia and influence blood cell formation (Driver, 1994; Dahl et al. 2001; Nielsen, 2004). Regarding toxicity of Zn, studies demonstrated reproduction toxicity in Acartia sp. (Hook and Fisher, 2002), D. magna (De Schamphelaere et al. 2004) and lipid peroxidation in juvenile galaxiid fish (McRae et al. 2016). In terrestrial animals, effects on fertility, low birth weight and skin irritation have been observed at high doses (Peterson et al. 2007). Furthermore, growth inhibition, development and oxidative damage have been reported in plants due to phytotoxicity of Zn (Reichman, 2002; Nagajyoti et al. 2010). Moreover, toxicity of zinc oxide (ZnO) nanoparticles particularly in acidic soil has been widely addressed in recent

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reviews in terrestrial animals and plants by inducing reactive oxygen species (ROS), (Ma et al. 2013; Rajput et al. 2018).

1.5.4 Developmental instability in studying effects on wildlife

There has been increased interest to understand the effects of ionizing radiation on wildlife. However, finding sensitive methods for detecting effects of environmental radioactivity in animals has been challenging due to environmental variables. Data on effects of radionuclides on wildlife is limited and current methods for finding such effects have showed lack of consistency.

Use of various developmental and reproductive endpoints such as mouthparts deformities (Savić-Zdravković et al. 2018), mentum and mandible size (Arambourou et al. 2015, 2020), reproduction (Arambourou et al. 2018), time to emergence (Arambourou et al. 2014, 2019, 2020) and reduced mass of tested animals (Arambourou et al. 2017, 2020) have been recommended to detect the effects of environmental contaminants in organisms. One of the approaches to investigate the impacts of environmental radiation on biota is measurement of developmental instability. It is most commonly measured by fluctuating asymmetry (FA), (Graham et al. 2010). Fluctuating asymmetry is defined as random phenotypic deviations from perfect bilateral symmetry in organisms and measured as variance of differences between the right and left body sides (Palmer and Strobeck, 1986). FA has been proposed as a tool to monitor and track any possible changes in a population of organisms, which might affect the entire ecosystem. The approach has been used in several studies as indicator of environmental stresses including radioactivity (Table 2), but lack of consistency has questioned the validity and usefulness of this approach. While several studies showed a high level of asymmetry due to exposure to environmental radioactivity (Møller, 1993a, 1993b; Gileva and Nokhrin, 2001;

Møller, 2002; Oleksyk et al. 2002; Smith et al. 2002; Oleksyk et al. 2004; Yavnyuk, et al. 2009; Makarenko et al. 2018), others found no significant effects on FA in the organisms tested (Beasley et al. 2012; Lajus et al. 2014; Fuller et al. 2017). It is not evident whether positive findings on FA are induced by the exposures studied or by confounding factors (Dongen, 2006). It is therefore important to understand the underlying mechanisms that lead to developmental instability in individu- als/species. More importantly usefulness of other endpoints needs to be investigated in comparison to developmental instability such as those suggested by OECD (2010): number of emerged adults, time to emergence and sex ratio. This is important because there is no evidence as to whether developmental instability would be a more sensitive indicator than other developmental endpoints.

Radioecology for boreal ecosystems : studies on transfer processes and effects on wildlife

Dissertations in Forestry and Natural Sciences

SOROUSH MAJLESI

Radioecology for Boreal Ecosystems:

Studies on Transfer Processes and Effects on Wildlife

RADIOECOLOGY FOR BOREAL ECO- SYSTEMS: STUDIES ON TRANSFER PROCESSES AND EFFECTS ON WILD-

LIFE

Soroush Majlesi

RADIOECOLOGY FOR BOREAL ECO- SYSTEMS: STUDIES ON TRANSFER PROCESSES AND EFFECTS ON WILD-

LIFE

ABSTRACT

ACKNOWLEDGEMENTS

LIST OF ABBREVIATIONS

LIST OF ORIGINAL PUBLICATIONS

AUTRHOR’S CONTRIBUTION

CONTENTS

1 INTRODUCTION TO ENVIRONMENTAL RADIOACTIVITY AND POSSIBLE ADVERSE EFFECTS ON WILDLIFE

1.1 ENVIRONMENTAL RADIOACTIVITY

1.2 RADIOECOLOGY

1.3 ELEMENTS RELEVANT TO RADIOACTIVE WASTE

1.4 TRANSFER OF RADIONUCLIDES TO ORGANISMS

1.5 EFFECTS AND TOXICITY OF ELEMENTS, RELEVANT TO RADIOACTIVE WASTE ON WILDLIFE AND ECOSYSTEMS