protectionofnon-human biota: history, conceptsand challenges

21112005

Protection of non-human biota:History, Concepts and Challenges

Deborah OUGHTON Norwegian University of Life Sciences, Aas, Norway

[email protected]

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Overview

� Introduction to Radioecology

� History of protection of non-human biota

� Ecological Risk Assessment

� Knowledge gaps and data needs

� Case Study Transfer: Central Asia and Fukushima

� Case study Effects: Earthworms

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�The study of the behaviour and impacts of radionuclides in the natural environment

� A multidisciplinary scientific discipline:

– Academic: ecology, ecotoxicology, geophysics, geology, limnology, biology, physiology, pedology, climatology, oceanography, …

– Risk oriented: radiological protection, health physics, regulation, human and ecological risk assessment, international harmonisation,…

Radioecology

Email: [email protected]://www.iur-uir.org/

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Radioecology: Research Applications 2015

�Nuclear new build (new ecosystems, new food chains, …)

�Waste management (new isotopes, new modelling, …)

�Nuclear fuel cycle (mining to decommisioning)

� TENORMS (e.g., oil scale, non-nuclear industries, ..)

� Accident Countermeasures (Chernobyl; Fukushima, ...)

�New regulations (environmental impact assessment,

� Isotope techniques – C-14, I-129, Pb-210, U-isotope ratios, Pu-isotope ratios, Al-26, B-10, (N-15, O-18)

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Environmental Chemistry

Nuclear Engineering

Radiological Protection

Ecotoxicology

Radiobiology

Ecology

Human orientatedNot radioactivity

Radioecology�Fragmentation from human

radiation protection and chemicalrisk assessment

�Lack of hypothesis driven research: monitoring and modelling

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International Commission for Radiological Protection (ICRP):

� Independent organisation in existence since 1927

� Initially provided guidance on medical uses of radiation

� Provides Recommendations and Advice on Radiological Protection, Emergency Prepardeness and Nuclear safety

www.icrp.org

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ICRP Three Stage Philosophy for Radiological Protection

� The Principle of Justification:

– Any decision that alters the radiation exposure situation should do more good than harm.

� The Principle of Optimisation of Protection:

– The likelihood of incurring exposure, the number of people exposed, and the magnitude of their individual doses should all be kept as low as reasonably achievable (ALARA), taking into account economic and societal factors.

� The Principle of Application of Dose Limits:

– The total dose to any individual from regulated sources in planned exposure situations other than medical exposure of patients should not exceed the appropriate limits specified by the Commission.

ICRP 103 (2007)

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The International Commission on Radiological Protection(ICRP)

“If man is adequately protected then other living things are also likely to be sufficiently protected” [ICRP, 1977],

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The International Commission on Radiological Protection(ICRP)

“The Commission believes that the standard of environmental control needed to protect man to the degree currently though desirable will ensure that other species are not put at risk. Occasionally, individual members of non-human species might be harmed, but not to the extent of endangering whole species or creating imbalance between species. At the present time, the Commission concerns itself with mankind’s environment only…." [ICRP, 1991],

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Lethal dose to different species from acute radiation doses

Figure 3.1 Comparative radiosensitivity of different organisms demonstrated as the acute lethal dose ranges (reproduced from UNSCEAR 1996).

Reproduction 20-100x more sensitive

100 101 102 103 104

Mammals

Birds

Higher plantsFishes

Amphibians Reptiles

Crustaceans Insects

Mosses, lichens, algae

Bacteria Protozoa

Molluscs Viruses

Acute lethal dose (Gy)

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Papers from Pentreath and Woodhead (1998- )

Report from International Union of Radioecologists (IUR) 2000

IAEA Report on ethical considerations (2003)

Issues:

Situations where humans are absent (e.g., disposal)

Not compatible with management of other environmental stressors

Needs to be demonstrated

Background: Towards a Framework for Radiological Protection of Non-Human Species

EU 6th-7th Framework Project s: FASSET, ERICA, PROTECT, STAR www.erica-project.org ; www.star-radioecology.org

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Emerging consensus that radiation protection needs to address the effects of ionising radiation on non-human species

ICRP 208 (2007) Environmental Protection - the Concept and Use of Reference Animals and Plants www.icrp.org

IAEA Safety Standards www.iaea.org

Requirement for enormous amount of information on transfer, uptake and effect of ionising radiation (especially for wild animals)

Background: Towards a Framework for Radiological Protection of Non-Human Species

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Flora

ManECOSYSTEM

Life support

Services

Linear Transfers Cyclic Transfers + Effects

Low doses Chronic exposuresMultiple stressors

PAST NOW

ManSources

Environment Environment

Biogeochemical

Radiation Protection: From Anthropocentric to Ecocentric

Brechignac, 2004; Brechignac et al. 2012

ContextDeb

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”Menace of the Nuclear Rabbits”*

� In 2003 rabbits were found to be burrowing in the Dounreay nuclear waste pits

� Concerns that they might be radioactive

� Concerns that they might be eaten by cats, humans, other wildlife

* Scotsman headline 12/6/2003

� Bye bye bunnys…

Rabbits nowWho’s next?*

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Overview

� Introduction to Radioecology

� History of protection of non-human biota

� Ecological Risk Assessment

� Knowledge gaps and data needs

� Case Study Transfer: Central Asia and Fukushima

� Case study Effects: Earthworms

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Environmental and Ecological Risk Assessment

�Environmental Risk – Risk to humans due to pollutants in the environment (US)

�Ecological Risk – Risk to non-human organisms (goal protection of the environment).

�Environmental Impact

Assessment – scientific and economic analysis of the impact of a technology or project on humans and environment.

www.epa.gov

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Isotope Laboratory Department of Plant

Environmental

Sciences

eRelease of radionuclides

Single effect endpoint:

Cancer induction (Sv)

Several effect endpoints:

Reproduction, sexual maturation

Human risk assessment Ecological risk assessment

Protection of individuals Protection of populations/communities

Human vs Ecological Assessment

One species Multiple species

Reference Man Reference Animals and Plants

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Risk Assessment Frameworks

�Planning/Hazard identification/Problem formulation

�Analysis/Exposure and dose-response evaluation

– Pathways

– Duration of exposure

– Dose-response curves

�Risk Characterisation

– Probability and severity of effects

– Evaluation of uncertainty

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Ecological Risk Assessment

What is the concentration of pollutants in the environment?

What organisms are exposed and to what doses?

Are the effects of those exposures harmful to populations, ecosystem function and/or biodiversity?

Discharge

Risk Quotient = Predicted Environmental Concentration (Dose)Predicted No Effect Concentration (Dose)

Oughton et al., JER, 2008

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� Deer� Rat� Bee� Earthworm� Pine tree� Grass

� Duck� Frog� Trout

� Flat fish� Crab

� Macroalga

ICRP « Reference Animals and Plants » - RAPs

� Typical, accessible, documented, various sizes and life cycles, measurable dose-effect

� Generic virtual entities to serve as points of comparison to assess exposure and effects

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NORWEGIAN UNIVERSITY OF LIFE SCIENCES

ERIC

A T

ool: R

efe

rence

org

anis

ms

ICRP ”

Refe

rence

Anim

als

and P

lants

” in r

ed

Deborah Oughton: MINA410 Environmental Radiobiology, 2015

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RAP and Reference Organisms

� A RAP is defined as:

– ‘ a hypothetical entity, with the assumed basic biological characteristics of a particular type of animal or plant, as described to the generality of the taxonomic level of Family, with defined anatomical, physiological and life-history properties, that can be used for the purposes of relating exposure to dose, and dose to effects, for that type of living organism.’

� A reference organism (as used in ERICA) is defined as:

– ‘a series of entities that provide a basis for the estimation of radiation dose rate to a range of organisms which are typical, or representative, of a contaminated environment. These estimates, in turn, would provide a basis for assessing the likelihood and degree of radiation effects.’

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Components within the assessment part

Activity concentrations in reference media

Activity concentrations in reference organism

Internal dose rate External dose rates

Total absorbed dose rate

- FREDERICA database - Natural background

CR

DCC

DCCs Occupancy factors

•Modelling transfer through the environment•Estimating doses to biota from internal and external distributions of radionuclides•Establishing the significance of the dose-rates received by organisms

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Transfer and exposure

(i) Inhalation of (re)suspended

contaminated particles or gaseous radionuclides.

(ii) Contamination of fur, feathers and skin.

(iii) Ingestion of lower trophic level plants and animals.

(iv) Direct uptake from the water column

(v) Ingestion of contaminated water (vi) External exposure.

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Dose Calculations to Organisms: Organism Habitats

� F = Dose rate that an organism will receive for the case of a unit concentration in environmental media (µGy h-1

per Bq l-1 or kg-1 (or Bq m-3 – terrestrial C, H, S, P only).

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Dose Calculations - example

�DCC = Dose Conversion Coefficient (mGy hr-1 per Bq kg-1)

� CR = Concentration Ratio (Bq/kg f.w. per Bq/l or Bq/kg)

� Kd = Distribution coefficient (l kg-1 )

Table H22 Habitats occupied by the ERICA marine reference organisms. In the case of several habitats for an organism, the equation is given for the habitat giving the highest dose-rate

Organism Habitat Equation

Phytoplankton 2

Macroalgae 3

Vascular plant 3

Zooplankton 2

Polychaete worm 4

Bivalve mollusc 3

Table H22 Habitats occupied by the ERICA marine reference organisms. In the case of several habitats for an organism, the equation is given for the habitat giving the highest dose-rate

Organism Habitat Equation

Phytoplankton 2

Macroalgae 3

Vascular plant 3

Zooplankton 2

Polychaete worm 4

Bivalve mollusc 3

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Dose Calculations to Organisms: Organism Habitats

� F = Dose rate that an organism will receive for the case of a unit concentration in environmental media (µGy h-1

per Bq l-1 or kg-1 (or Bq m-3 – terrestrial C, H, S, P only).

� PNEDR = Predicted No Effect Dose Rate (10 uGy/hr)

� EMCL = Environmental Media Concentration Limit

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Biological Effects –KJ350

Deborah Oughton

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Experimental measurement – any effect or endpoint

wR

WR = radiation weighting factor

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RBE and Weighting Factors for Non.human species

ERICA default weighting factors:

� alpha = 10

� low energy beta, (e.g., T) = 3

0%10%20%30%40%50%60%70%80%90%

100%

0.1 1 10 100

RBE value

Cum

ulat

ive

wei

ghte

dpr

obab

ility

Best-Estimate Centile 5% Centile 95%

Alpha – no more details

Ra223 Pu239 Pu238 Po212

Po210 Pb212 He-4 Gd148

Bi212 Am241

α particles

0%10%20%30%40%50%60%70%80%90%

100%

0.1 1 10 100

RBE value

Cum

ulat

ive

wei

ghte

dpr

obab

ility

Best-Estimate Centile 5% Centile 95%

Alpha – no more details

Ra223 Pu239 Pu238 Po212

Po210 Pb212 He-4 Gd148

Bi212 Am241

α particles

Chambers et al., 2006; Garnier-Laplace et al., JER, 2008

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Case1 : Fukushima, distribution of releases between land and sea

Atmospheric deposition

１

Mid-March

（5〜30 P Bq）

Direct discharge２

After late-March

(3〜15 P Bq)

small source today

Through river runoff３

Through underground water flow

４

small and continues

small and continues?

80% Fukushima

contamination in ocean

There are still some

uncertainties on “where” and

“how much” of different

radionuclides were released

to the environment.

P (peta)

= 1015

Slide courtesy of Ken Buessler, www.whoi.edu

One year history of cesium-137 in ocean immediately off Fukushima

Levels prior

to March 11

At nuclear power plant

Ocean Cs levels peak on April 6th

- possible reproductive effects

and mortality for marine biota

Levels of

concern

for

seafood

Highest

ocean levels

post

Chernobyl

US drinking

water limit

- Fukushima NPP

represents unprecedented

release of radionuclides to

the ocean

- levels decreased rapidly,

then leveled off

- so there is a continued

source

-The majority of seafood

below permissible levels

for consumption

Persistently high levels in

some marine organisms

one banana

April 1 June 1 Aug 1 Oct 1 Dec 1 Feb 1

------------------ 2011 -------------------------------- ----2012---

Data from TEPCOSlide courtesy of Ken Buessler, www.whoi.edu

What types of fish are

most contaminated?

- bottom fish

& freshwater fish

- still high after 1 year

- variability unpredictable

- 18% of fish reported

are above limit

Data source- Japan Fisheries

Buesseler, Science , 2013

Ken Buesseler

WHOI

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Bjørn Olav Rosseland:

Reiser i 2008 med miljøgifter

og fiskevelferd som mål.

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Photo. B.O. Rosseland

Example of Dose Assessment: Central Asian Mining sites

Stalin’s Uranium mining 1952-58

Oughton et al., JER, 2013


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Ura

niu

m m

inin

g a

nd t

aili

ng in f

orm

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Sovi

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Unio

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E

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Fieldwork in Kazakhstan in June 2006

ChinaTadjikistanUzbekistan

Kazachstan

Kirgisistan


ICRP T

err

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Digmai Site, Tajikistan

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Modelled external doses in good agreement (factor 2) of site measurements

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Estimated total doses (µGy/hr) to reference terrestrial organisms Kurday (mean

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0

10

20

30

40

50

60

70µ

Gy/h

y

Ra-226

U-238

Th-234

Pb-210

Ra-228

Th-228

U-234

Oughton et al., 2013

Internal doses: 73-95% of totalRa-226 dominated at all sites

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Dose Conversion Co-efficient (DCC) and Daughter radionuclide DCC

�Daughter nuclides are included in the dose conversion coefficients of their parents, if their half-lives are shorter than 10 days (assuming that the daughters are in equilibrium with parents).

– Pb-210 (Bi-210)

– Ra-226 (At-218, Po-218, Bi-214, Pb-214, Rn-222, Po-214)

– Ra-228 (Ac-228)

– Th-228 ( Po-216, Tl-208, Bi-212, Pb-212, Rn-220, Po-212, Ra-224)

– Th-234 (Pa-234m, Pa-234) U-235 (Th-231)

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Sampling of vegetation

Photo: B.O. Rosseland

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Good agreement between ERICA Ra-226 and U Concentration Ratios in ERICA tool and site plants

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Total dose (uGy/hr)

Reference grasses

Site vegetationKurday

U-238 0.14 0.03 - 0.77Ra-226 4 2.0 - 3.3

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Doses to Biota: Kadji-Sai U mining site, Kyrgystan (µGy/hr)ERICA Assessment Tool

Soil Activity concentrations CR wormU238/234 5700 Bq/kg 8.8 * 10-3

Ra-226 5000 Bq/kg 9.0 * 10-2

Internal dose to wormDose to gut 2-4 ordersof magnitude greater

Default ERICA database CROne data point UNo data Ra

Oughton et al, JER, 2013

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Metal soil concentrations (mg/kg)

Metal Kurday Issyk-Kul Digmai(n=2)

LEL* (mg/kg)

Cu 21 – 91 26 – 46 53 - 79 3.4 - 50

Cr 11 – 66 nd 51 - 59 0.4 – 81

Ni 20 – 54 16 – 34 10 – 13 13 – 100

As 9 – 53 9 – 33 50 - 58 5.7 – 60

Mo 0.64 – 102 n/a n/a 3 - 190

Cd 0.29 – 0.94 0.35 – 1.2 n/a 0.8 – 20 44

*Environmental Quality Standards based on Lowest Effect Levels (LEL) (RIVM, 2001; EPA, 2004).

Identified a potential for multiple stressor issues

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Dose

s to

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Photo. B.O. Rosseland

Dead lake: Kurday Kazakstan

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Estimated doses to reference biota, Kurday, Aquatic Environment (µGy/hr)

0

2

4

6

8

10

12

14

16

18

20

Ra-226

Po-210

0

500

1000

1500

2000

2500

3000

3500

Uranium

U-238

Oughton et al., 2013

Internal doses dominate

U site specific doses 100x less for plants

Site activity measurements

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Estimated doses (µGy/hr) to reference aquatic organisms at Issyk-Kul Lake, Kyrgystan

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Po-210 internal doses dominatedfor most organismsU isotopes dominated for plants

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Metal Water concentrations (ug/L)

Metal Kurday*Issyk-Kul

TabosharDutch target

Dutch intervention

Cu 3.2—6.2 (7.8) <2 na 15 75

Mn 5—80 (2000) 1 13 50 2000

Cr 0.27 – 5.2 (1.45)

1.5 3.5 1 30

Ni 22—71 (101) 5.5 3.7 20 52

As 0.9—2.6 (23) 16 26 10 60

Mo 9—173 (134) na 35 5 30049

* Concentration in a sample collected from the Artesian well is given in brackets.

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Main Sources of Numerical Uncertainty in Environmental Transfer and Dose Calculations


What organisms are exposed and to what doses?

Are the effects of those exposures harmful to ecosystem function and biodiversity?

Discharge

Transfer factorsConcentration RatiosWater-sediment partitioningSpeciationSpatial and temporal variationRadiation weighting factorsInternal doses (inhomogeneity)

Range from 1 - 5 orders of magnitude

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Oug

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et a

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Natural background

10-2

Dose rate (µGy/h)10-1 1 10 100 1000 10000

Nuclear installation in normal operation

TERRESTRIAL PLANTS

MOSSES, LICHENS, MUSHROOMSAQUATIC PLANTS

BACTERIAPROTOZOA

BIRDS

CRUSTACEANSMOLLUSCS

FISHES

INSECTS

MAMMALS

AMPHIBIANS

REPTILESEnough data to derive « no effect dose rates »

No data

Experimental investigations of dose-effects relationships (external)

Radiation effects on wildlife: Knowledge Gaps

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� A few species studied� Data mostly derived from short-term studies � Data mostly derived from acute doses (and dose rates) � Data essentially derived from external exposure situations (γirradiation) � Data essentially derived from observations up to individual level

State of the art on radiation effects on animals and plants

� More species (biodiversity)� Long-term (trans-generational) � Low doses and dose rates

� Internal contamination

� Observations at population, community and ecosystem level

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Biological Effects –KJ350

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Knowledge Gaps and Extrapolation

�Acute to chronic

�High to low dose/dose rate

�Species to species

� Laboratory to field

�Sub-lethal to individual to population

�Single contaminant to mixtures of stressors

�External to Internal

�High to low LET

”Safety Factors”

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Effect Analysis and Risk Characterisation


What organisms are exposed and to what concentrations/doses?


Discharge

Vary according to:SpeciesLife-stage EndpointTissue sensitivityGenetic SusceptabiltyExposure ScenarioMulti-contaminants

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� Cancer is not a problem for wildlife organisms

� In nature, protection of the population - not the individual - is most important

� Focus on reproduction – why?

– Reproduction determines not only the fate of the single organism but is essential for maintaining the population and hence the balance of higher ecological units

– Reproduction is one of the more radiosensitive endpoints

Case: Chronic irradiation of earthworms (Eisenia fetida)

Case Study: Ecologically Relevant Effects of Ionizing Radiation on Earthworms

Why me?

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� Rat� Bee� Earthworm� Pine tree� Grass

� Duck� Frog� Trout

� Flat fish� Crab

� Macroalga

Reference organisms:ICRP « Reference Animals and Plants »

• Recognized test species in chemical toxicity studies; standardised tests (OECD)

• Potentially high exposure to radionuclides

• Important role in soil ecosystems

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Isotope Laboratory Department of Plant

Environmental

Sciences

Why me?

Important role in the food web Important for the soil fertility

Eat dead organic material

•Increases the bioavailability of nutrients for other organisms

They make burrows in the soil

•Increase the aeration and water drainage

•Mixing organic and inorganic components of the soil

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“An earthworm is not just an earthworm”

� The total number of species is estimated to exceed 2000

� Three major ecological groups of earthworm have been identified based on the feeding and burrowing behaviours of the different species.

E. fetida

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Earthworm anatomy and physiology

� Earthworms are segmented

� The principal excretory organs are the nephridia

� They have no specialized respiratory organs: They respire over the whole body surface

– Thin cuticle covered with mucus

� Coelomocytes; immune cells in the coelom

� The circulatory system is closed with a blood vessel running along the dorsal and ventral surface of the digestive tract

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Reproduction in earthworms

� Esenisa fetida are hermaphrodites with separate testes and ovaries that function simultaneously

� During mating they crossfertilize

� Spermatozoa are transferred to spermatechae

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Life cycle: Eisenia fetida

� The life-cycle of E.fetida is relatively short

– approximately 11 to 16 weeks from cocoon to sexual maturity (20°C)

� The life span is rather long

– E.fetida has been kept in the laboratory for about 4 ½ years

– Can be reproductively active for more than 500 days

2-5 cocoons per worm per week

1-6 hatchlings per cocoon

Growth and sexual maturation: 8-12 weeks

Adult

Juvenile

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Sou

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FIG

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: Fa

cilit

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r Lo

w D

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Rate

Gam

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2009

2012


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Main objectives:

� Establish dose (rate) response relationships for reproduction endpoints in two subsequently exposed generations (F0 and F1).

– Cocoon production rate

– Cocoon hatchability

– Number of hatchlings

– F1 growth and sexual maturation rate

�Hypothesis: that 4 week exposure (the standard OECD test) would underestimate reproduction effects (spermatogenesis)

Important for population dynamics

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EXPERIMENTAL SETUP - EXPOSURE

Life stage, generation Exposure time

Cocoons 3 weeks

Adult (F0)reproduction

13 weeks

Juvenile (F1)

growth /maturation

11 weeks

Adult (F1)reproduction

13 weeks

38

14

5691 21 35

24

F1 Growth and maturation Adult F1 ReproductionAdult F0 reproduction

Hatching of F1 juveniles

9

0

13

28 56

4 8 3 5 8 11 16 20

63 77 112 140 168

Dose rates: 0.01 – 40 mGy/hr

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Specific endpoints

Generation Endpoint

Adult (F0), Adult (F1)

Viability, weight, morbidity

Number of cocoonsHatchability

Number of hatchlings (F1)

DNA damage in somatic,spermatogenic cells and sperm

Hatchlings (F1) ViabilityGrowth rateMaturation rate

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• The most sensitive endpoint was cocoon hatchability.

• Effects took several months to appear at 11 mGy/h, and standard reproduction tests for Eisenia fetida (4 weeks) are therefore insufficient

0% 0%

0

20

40

60

80

100

1-4 5-8 9-13Weeks of exposure

% H

atch

abili

ty

Control 0.18 mGy/h 1.7 mGy/h 4.2 mGy/h 11 mGy/h 43 mGy/h

Hatchability of F0 cocoons

Hertel-Aas et al., Radiation Research, 2007

0

10

20

30

40

50

60

70

Control 0.19 mGy/h 1.7 mGy/h 4 mGy/h 11 mGy/h 43 mGy/h

# F

1 ha

tchl

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per

adu

lt F

0

**

*

**

• Reduction in the total number of

offspring produced by each F0

MAIN RESULTS: F0 GENERATION

EDR10 3.2 mGy/h

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Life-cycle trait variations in earthworm species

�Dendrobaena octaedra

– Epigeic

– Reproduction – pathenogenesis (clonal, rapid adaptation)

– Frost tolerant

� Lumbricus terrestris

– Anecic

– Sperm storage up to 12 months after mating

– Cocoon incubation median 1.5 yrs (up to 5 yrs)

– 1 hatchling per cocoon

68

•Population dynamic modelling•Identify candidates and endpoints for future effect studies•Field studies

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Population effects

Data related to individual organisms : what link to population ?

• Individual mortality => mortality rate => population density

• Fertility => reproduction rate => population density

Toxicology Ecology

Ecotoxicology

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Wildlife defies ChernobylradiationBy Stephen MulveyBBC News

« It contains some of the most contaminated land in the world, yet it has become a haven for wildlife- a nature reserve in all but name. »

20 April 2006

Chernobyl 'not a wildlife haven'

By Mark Kinver Science and nature reporter BBC News

« The idea that the exclusion zone around the Chernobylnuclear power plant has created a wildlife haven is not scientifically justified, a study

says. »

14 August 2007

What is Harm? (Slide courtesy of Tom Hinton)

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Uncertainties and Variabilities in Effect Analysis


What organisms are exposed and to what concentrations/doses?


Discharge

Vary according to:SpeciesLife-stage EndpointTissue sensitivityGenetic SusceptabiltyExposure ScenarioMulti-contaminants

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Summary: Challenges within Ecological Risk Assessment

� Lack of data on radionuclide transfer and ecosystem distribution

� Variation in species-sensitivity and life-history stages

�Multiple stressors

� Lack of experimental data on ecologically-relevant effects

�Mechanisms and biomarkers

� Adaption, acclimatization, adaptive response

� Population and ecosystem effects

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Summary: Human vs Ecological Assessment

Human Ecological

Cancer endpoint Multiple endpoints

One species Many species

Unit of protection Unit of protection

individual population

Doses Sv Doses Gy

Reference person Reference Animals and plants

Deterministic and Deterministic effects

stocastic effects73

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Quest

ions

?


protectionofnon-human biota: history, conceptsand challenges

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