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The biological effects of ionising radiation on Crustaceans: A review

Neil Fuller, Adélaïde Lerebours, Jim Smith, Alex Ford

To cite this version:

Neil Fuller, Adélaïde Lerebours, Jim Smith, Alex Ford. The biological effects of ionis- ing radiation on Crustaceans: A review. Aquatic Toxicology, Elsevier, 2015, 167, pp.55-67.

�10.1016/j.aquatox.2015.07.013�. �hal-01978333�

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AquaticToxicology167(2015)55–67

ContentslistsavailableatScienceDirect

Aquatic Toxicology

jo u r n al h om ep ag e :w w w . e l s e v i e r . c o m / l o c a t e / a q u a t o x

The biological effects of ionising radiation on Crustaceans: A review

Neil Fuller

a

, Adélaïde Lerebours

a

, Jim T. Smith

b

, Alex T. Ford

a,∗

aInstituteofMarineSciences,SchoolofBiologicalSciences,UniversityofPortsmouth,FerryRoad,Portsmouth,HampshirePO49LY,UK

bSchoolofEarth&EnvironmentalSciences,UniversityofPortsmouth,BurnabyBuilding,BurnabyRoad,Portsmouth,HampshirePO13QL,UK

a r t i c l e i n f o

Articlehistory:

Received13May2015

Receivedinrevisedform15July2015 Accepted23July2015

Availableonline26July2015

Keywords:

Ionisingradiation Crustacean

Environmentalradioprotection Radionuclide

a b s t r a c t

Historicapproachestoradiationprotectionarefoundedontheconjecturethatmeasurestosafeguard humansareadequatetoprotectnon-humanorganisms.Thisviewisdisparatewithothertoxicants whereinwell-developedframeworksexisttominimiseexposureofbiota.Significantdatagapsformany organisms,coupledwithhighprofilenuclearincidentssuchasChernobylandFukushima,haveprompted there-evaluationofourapproachtowardenvironmentalradioprotection.Elucidatingtheimpactsofradi- ationonbiotahasbeenidentifiedaspriorityareaforfutureresearchwithinbothscientificandregulatory communities.Thecrustaceansareubiquitousinaquaticecosystems,comprisinggreaterthan66,000 speciesofecologicalandcommercialimportance.Thispaperaimstoassesstheavailableliteratureof radiation-inducedeffectswithinthissubphylumandidentifyknowledgegaps.Aliteraturesearchwas conductedpertainingtoradiationeffectsonfourendpointsasstipulatedbyanumberofregulatorybod- ies:mortality,morbidity,reproductionandmutation.Amajorfindingofthisreviewwasthepaucityof dataregardingtheeffectsofenvironmentallyrelevantradiationdosesoncrustaceanbiology.Extremely fewstudiesutilisingchronicexposuredurationsorwildpopulationswerefoundacrossallfourendpoints.

Thedoselevelsatwhicheffectsoccurwasfoundtovarybyordersofmagnitudethuspresentingdiffi- cultiesindevelopingphyla-specificbenchmarkvaluesandreferencelevelsforradioprotection.Based onthelimiteddata,mutationwasfoundtobethemostsensitiveendpointofradiationexposure,with mortalitytheleastsensitive.Currentphyla-specificdoselevelsandlimitsproposedbymajorregulatory bodieswerefoundtobeinadequatetoprotectspeciesacrossarangeofendpointsincludingmorbidity, mutationandreproductionandexamplesarediscussedwithin.Thesefindingsservetoprioritiseareas forfutureresearchthatwillsignificantlyadvanceunderstandingofradiation-inducedeffectsinaquatic invertebratesandconsequentlyenhanceabilitytopredicttheimpactsofradioactivereleasesonthe environment.

©2015TheAuthors.PublishedbyElsevierB.V.ThisisanopenaccessarticleundertheCCBYlicense (http://creativecommons.org/licenses/by/4.0/).

Contents

1. Introduction...56

2. Radiation-inducedmutationincrustaceans...57

3. RadiationimpactsonmorbidityinCrustaceans ... 58

3.1. Radiation-inducedimpactsongrowth&respiration...60

3.2. Theeffectsofionisingradiationonthebehaviour&histopathologyofCrustaceanspecies ... 61

4. TheeffectofionisingradiationonreproductioninCrustaceans...62

5. Radiation-inducedmortalityinCrustaceans...62

6. Conclusions...63

Conflictofinterest...64

Acknowledgements ... 65

References...65

Correspondingauthor.

E-mailaddress:alex.ford@port.ac.uk(A.T.Ford).

http://dx.doi.org/10.1016/j.aquatox.2015.07.013

0166-445X/©2015TheAuthors.PublishedbyElsevierB.V.ThisisanopenaccessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).

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1. Introduction

Therenewedinterestinnuclearpowerasalowcarbonemis- sion energy source coupled with concern regarding past and potential nuclear accidents dictate that elucidating the impact of radionuclides on the environment is a global issue. Tradi- tionalapproachestoradiological protectionof theenvironment are based on the assumptions that the standards of environ- mental control needed to protect humans would be adequate toprotectotherspecies (Copplestoneet al.,2004;International Commission on Radiological Protection (ICRP, 1977). However thisanthropocentric approachis nolongeracceptedduetothe paucity of information regarding the effects of ionising radia- tion on non-human biota (Pentreath, 1998; Thompson, 1988), the varying sensitivities of different species and developmen- talstagestoradioactivecontaminants(Haggeretal.,2005)and the existence of habitats in which organisms may be exposed todosesabove thepermissiblelimitsfor humans(Copplestone etal.,2001).Assessingthebiologicalimpactofionisingradiation onnon-humanbiotahasbeenidentifiedasanecessaryapproach towardsprotectingandmitigatingtheimpactsoffutureradioac- tivereleaseson theenvironment by a number ofinternational directives(e.g.,ERICAandPROTECT[Howardetal.,2010;Larsson, 2008]).

Thepresenceofionisingradiationintheenvironmentoriginates from both natural and anthropogenic sources. Natural sources includecosmicradiationoriginatingfromoutsidethesolarsys- temandprimordial radionuclidesarisingfromstellarprocesses (Smith&Beresford,2005).Themajorityofanthropogenicradionu- clidesintheenvironmentarederivedfromthreemajorsources:

nuclear weapons testing, nuclear disasters and permitted dis- charges from nuclear reprocessing plants (Aarkrog, 2003). The aquaticenvironment representsan importantsinkfor radionu- clides(Avery,1996),sincethemajorityofdepositionofradioactive wastefromnuclearfacilitiesisin liquidformanddepositionof atmosphericfalloutinoceanecosystemsisapproximatelytwo-fold higherthanin terrestrialsystems(Burton,1975).Radionuclides present in the terrestrial environment may also contribute to radioactivityin aquaticenvironmentsviarun-off. For137Cs and

90Sr,thetwomajorman-madecontributorstoworldwideradi- ation doses (IAEA, 1995), approximately2 and 9% of thetotal landinventorieswillbetransported toaquaticsystems respec- tively via this pathway (Yamagata et al., 1963). However, the bioavailabilityofradionuclidesderivedfromrun-offisoftenlimited by the binding of such radionuclides to particulates and sub- sequentsedimentation(Aarkorg,2003).Furthermore,catchment andsoilcharacteristicshave beendemonstratedtosignificantly impactthemobilityofradionuclidesbythispathway(Smithetal., 2004).

Directdisposalofsolidradioactivewasteintothemarineenvi- ronmentwasconductedovera48yearperiodfrom1948to1993, leading to dumping of approximately 85 PBq (1×1015 Bq) of radioactivematerial(IAEA,1999).Themajorityofdumpedwaste waslow levelsolidwastedepositedintheNEAtlanticanddis- posalofreactorsbytheformerSovietUnionintheKaraSea,being 53.4and43.3%oftotaldumpedactivityrespectively(IAEA,1999).

Radiologicalmonitoringofdumpsitesbyanumberoforganisations revealed negligible impacts on overall radioactive contamina- tionandemphasisedthegreaterinfluenceofatmosphericfallout, althoughelevatedradionuclidelevelswereobservedinthevicinity ofsomedumpsites(i.e.,Baxteretal.,1995).

Permittedreleasesfromnuclearreprocessingsitesrepresenta significantsourceofanthropogenicradionuclidestotheworld’s oceans. For example, the Sellafield nuclearspent fuel reproce- ssingsitelocatedinCumbria,UnitedKingdom,generatedaliquid radioactiveeffluentof6.649×105 GBqbetaandgammaemitters

(excludingtritium) over a four yearperiod from 1995to1999 (EuropeanCommission,2001).Suchdischargesaredetectablein mostareasoftheNEAtlanticandintheArcticOcean,represent- ingasignificanttransferofradioactivecontamination(Kershaw&

Baxter,1995).MajorcatastrophessuchastheexplosionattheCher- nobylNPPandtheT ¯ohokuearthquake–tsunamiattheFukushima Dai-ichi NPP led tolarge scale releases of radioactive material into theenvironment (Buesseler et al., 2012). Estimatesof the overall input of 137Cs to the world’s oceans as a consequence oftheChernobylincident are15–20PBq(Aarkroget al.,2003).

Finallytheuseofradioisotopesinmedical,industrialandscien- tificinstitutionsleadstocontaminationofthemarineenvironment typically orders of magnitude lower than other major sources (Aarkrogetal.,2003).

Althoughtheneedforenvironmentalradioprotectionframe- workshaslongbeenestablished,(PentreathandWoodhead,1988;

Pentreath, 1998) a lack of scientific consensus regarding the doses at which significantbiological effects occur(Beresford &

Copplestone,2011)andthedisparitybetweenresultsoflabora- torybasedexposuresandfieldstudies(Garnier-Laplaceetal.,2013) haveprecludedaradiologicalriskassessmentfortheenvironment.

Thisprovidesacontrastwithotheranthropogeniccontaminants wherein protection frameworks and concepts (i.e., the Ecolog- ical Risk Assessment concept) are well developed (Bréchignac, 2003).Anoverviewoftheeffectsofionisingradiationonaquatic invertebrates has previously been carried out by Dallas et al., (2012).Thispaperadoptsa phyla-specificapproach inorderto provideamoredetailedanalysisofeffects,andprioritiseresearch needs for the Crustacea,a group of organisms that have been identifiedas keymodelsforthedevelopmentof environmental radioprotection frameworks (ICRP, 2008).Members ofthe sub- phylumCrustaceaarethedominantcomponentsofglobalaquatic ecosystems and comprise more than 66,000 species (LeBlanc, 2007).Theseorganismsprovideanarrayofcommercialandecolog- icalservicesandareusedbothdirectlyforhumanconsumptionand asafoodsourceforothercommerciallyimportantspecies(Benzie, 2009).Duetotheirubiquityinaquaticenvironmentsandwellchar- acterizedbiology,amarinecrustaceanofthefamilyCancridaehas beenselectedasoneoftheICRP’sreferenceanimals(ICRP,2008).

Referenceorganismswillbeusedasabasistodevelopenviron- mentalradioprotectionmeasures,andareconsideredecologically representativeofaspecifiedgroupofplantsoranimalswithbio- logicalcharacteristicsamenabletostudy(ICRP,2008).Tosupport thedevelopmentofrobust,applicableecologicalbenchmarkval- uesforenvironmentalradioprotectionitisnecessarytoreviewand identifyresearchneedsforradiobiologicalstudiesintheselected referenceorganisms.Thispaperaimstoreviewtheavailablelit- eratureregarding the biological effects of ionisingradiation on thecrustaceansubphylum,drawcomparisonsacrossbiomarkers andassess anygapsinknowledge inthecontextof developing doselevelsforradioprotection.Emphasiswillbeplacedonstudies employingthefourbiologicalendpointsasoutlinedbyCopplestone etal.,(2008)andRealetal.,(2004);mutation,morbidity,reproduc- tivecapacityandmortality.

Thescopeoftheliteraturesearchwaslimitedtoaquaticcrus- tacean species exposed to any form of ionising radiation. The FREDERICAradiation effects database(Availableat http://www.

frederica-online.org) along with other search engines (Google Scholar,ScienceDirectandWebofScience)wasusedasatoolto extractreferencesrelatingtothefourumbrellaendpointsselected inthisreview.TheFREDERICAdatabasecontainsreferencesfrom anumberofEuropeanCommissionfundedprojects(i.e.,EPICand FASSET)from1945to2007.Allreferenceswithinthisdatasetare subjecttoreviewbasedontheadequacyandreproducibilityofthe study(Copplestoneetal.,2008).

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N.Fulleretal./AquaticToxicology167(2015)55–67 57

Fig.1.Illustrationoftherelationshipbetweencontaminantexposureandecosystemquality.AdaptedfromJha(2008).Fig.1reproducedwithpermissionfromJha(2008).

2. Radiation-inducedmutationincrustaceans

Forthepurposeofthisreview,amutationisdefinedas“Achange inthechromosomeorgenesofacellwhichmayaffectthestructure anddevelopmentoftheresultantoffspring”(Copplestone,2008).

Chromosomalandgeneticchangeshavebeenpostulatedbyanum- berofauthorstohavesignificantecologicalimplicationsathigher levelsofbiologicalorganisation(SeeFig.1(AndersonandWild, 1994;Depledge,1998;Jha,2008).

Despiteevidencesuggestingtheclastogenic(capacitytocause chromosomal aberrations) and mutagenic potential of ionising radiationobservedinarangeoforganismsincludinghumans(Lucas etal.,1992),fish(AnbumaniandMohankumar,2012;Kligerman etal.,1975;Pechkurenkov,1991)andmolluscs(AlAmrietal.,2012), thereisapaucityofinformationwithintheliteratureregardingthe crustaceansubphylum.Indeed,theFREDERICAdatabasecontain- ingover30,000dataentriescollatedfromanumberofinternational radiationeffectsdirectivescontainsnodataregardingmutationin crustaceanspeciesoverchronicdoserangesof0–>10,000␮Gy/hr-1 (SeeTable1Copplestoneetal.,2008).Similarly,the2008ICRPpub- licationintroducingtheconceptofreferenceanimalsandplants reportednoavailabledataforchromosomaleffectsincrabspecies (ICRP,2008),reiteratingthelackofstudiesinthisarea.

Fieldstudieshavesuggestedthatmutationmaybeasensitive endpointof radiation-induced effects incrustaceanspecies. For example,Florouetal.,(2004)assessedchromosomalaberrationsin microfaunacollectedfromgeothermalspringareasontheisland ofIkaria, Greecewhere maximumdoseratesofnatural gamma emittersinsedimentswere9.6mGyyr−1(∼0.001mGy/hr−1).These values are substantially elevated above the reported mean of 0.07mGyyr1(∼0.008␮Gy/hr1)forcoastalsedimentsinGreece (FlorouandKritidis,1992).Anelevatedlevelof cellsdisplaying chromosomeaberrations(3.8%)wasrecordedinpopulationsofthe amphipodcrustaceanMelitapalmata collectedfromtheseareas comparedwithcontrolsites(1.5–1.7%).Theauthor(Florouetal., 2004)attributedthis toincreasednatural doseratesof gamma andnaturalalphaemitters,whichwerealsoincreasedaboveback- ground levels in spring areas (14–26Bql−1 of 222Rn compared with 1.3–7Bql−1 in control areas). These dose values fall sig- nificantlybelow proposedenvironmentalprotectionbenchmark valuesprovidedbyanumberoforganisations(SeeTable2)sug- gestinginductionofsignificantbiologicaleffectsbelowdosesthat are consideredtohave nodeleteriouseffects at thepopulation level. However,thebiotainhabiting geothermalspringhabitats aretypicallyspecies-poorandsubjecttomultiplestressorsinclud- ingelevatedtemperaturesinwinterperiods(Flourouetal.,2004)

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Table1

CollationofavailablechronicradiationeffectdataanddatagapswithinthesubphylumCrustacealocatedintheFREDERICARadiationEffectsDatabase.X=availabledata -=nodataavailable.ReproducedwithpermissionofCopplestoneetal.,(2008).

DoseRateRange(␮Gy/hr−1)

0–50 50–100 100–200 200–400 400–600 600–1000 1000–5000 5000–10,000 >10,000

Morbidity X X X X X

Mortality

Mutation

ReproductiveCapacity

andextremesofpHandchemicaltoxicants(Dugganetal.,2007).

Thus,theobservedcytogeneticresponseinspringbiotamayhave beenduetothecomplexenvironmentalconditionspresentatthe studysitesasopposedtothedirecteffectsofionisingradiation.

Thishighlightstheinherentdifficultiesinfieldradioecologystud- ies(Salbu,2009)andtheimportanceofquantifyingtheindividual contributionofstressorsinenvironmentswhereabioticpressures mayactsynergistically(Dallasetal.,2012).Theaforementioned paperrepresentstheonlystudyofnaturalcrustaceanpopulations usingmutationasanendpoint.Thepreviouslydiscussedlimita- tionspresentdifficultiesindrawingconclusionsfromthisstudy asobserved cytogeneticeffects cannot bedirectlyattributedto ionisingradiation.

Laboratory studies assessing radiation-induced mutations in crustaceans typically involve acute high doses that are unrep- resentative of environmental exposures. Such studies have demonstratedtheabilityofionisingradiationtoinducechromo- somalaberrationsincrustaceanspecies.Tsytsugina(1998)exposed embryosoftwocrustaceanspecies,IdoteabalticaandGammarus oliviitodosesof0.5–5Gyfromarangeofradionuclidesandchem- icalmutagens (LeadAcetate andChlorophene) and scoredcells onthepresenceofchromosomal abnormalities.Themeannum- berofcellswithchromosomalaberrationsincreasedconcomitant withradiationdose.Furthermore,theauthordescribedcharacter- istictypesofaberrationsproducedbythetwotoxicantswhichmay beusedtodistinguishbetweentheeffectsofindividualstressors.

Forexample,ionisingradiationwasshowntoelicitchromosomal damageintheformofsingleandtwinfragments,whereas,sin- gle and twin bridges were more commonly observed in those embryosexposedtochemicaltoxicants.Thedistributionofaber- rationsbetweencells wasalsofoundtocorrespondtodifferent statisticaldistributionsdependentonthetoxicant,underpinning thepotentialofthismethod.However,thekaryotypeofcrustacean speciesisoftenreportedtobeunamenabletocytogeneticstudy (Salemaa,1985)duetothetypicallysmallsizeandhighdiploid numbersofchromosomes(White,1973).Thismayprecludeappli- cationofthismethodtonaturalpopulations.

Recentapproachestoassessingradiation-induced genotoxic- ityinaquaticinvertebrateshaveinvolvedmonitoringlevelsofthe expressionofgenesthatareinvolvedinDNAdamagerepairpath- ways(AlAmrietal.,2012;Hanetal.,2014a;Hanetal.,2014b;Won andLee,2014).Forexample,Hanetal.,(2014b)exposedcultures oftheintertidalcopepod,Tigriopusjaponicustogammaradiation from137CsandmonitoredmRNAexpressionofthreeDNArepair genes:Ku70(Xrcc6),Ku80(Xrcc5)andDNA-PK.Thesethreegenes areintegraltothenon-homologousendjoining(NHEJ)DNArepair pathwayinvolvedinthedetectionandrepairofradiation-induced doublestrandbreaks(DSBs)(Mahaneyetal.,2009).Expressionof thethreegeneswassignificantlyelevatedwithrespecttocontrols in200Gyexposedorganisms,suggestinginductionofDSBsatthese doselevels(Hanetal.,2014b).Thepotentialofthisapproachasa biomarkerforgenotoxicityincrustaceanspecieswasemphasised byWonandLee(2014)whoreportedadosedependentincreasein mRNAexpressionofthesegenesinanothercopepodspecies,Para- cyclopinanana(SeeFig.2).However,bothofthesestudiesuseddose

Fig.2.Dose-dependentincreaseinmRNAexpressionofthreegenesinvolvedinthe non-homologousendjoiningpathwayforDNArepairingammaradiationexposed culturesofthecopepod,Paracyclopinanana.Fig.2reproducedwithpermissionof Won&Lee(2014).

levelssignificantlyhigherthanthoseencounteredinradioactively contaminated environments (except perhaps in the immediate aftermathofamajornuclearaccident).Furthermore,intheformer study (Han et al., 2014b)gene expressionwas only monitored atdoselevelsof150and200Gy,despiteinductionofsignificant biologicalimpactssuchasareducedfecundityinT.japonicusat three-foldlowerdoselevels(50Gy).Alterationstogeneexpression patternsandmolecularlevelresponsesareoftenreportedtobesen- sitiveindicatorsofcontaminantexposureinaquaticinvertebrate species (Lee et al., 2006). A recent study supported the previ- ousstatement, reportingsignificantDNAalterations in Daphnia magnafollowingexposureto137Csdosesaslowas0.007mGyh−1 usingrandomamplifiedpolymorphicDNA-polymerasechainreac- tion(RAPD–PCR) methods(Parisotet al.,2015).Molecularlevel responseswereevidentatbothlowerdosesandshorterexposure durationsthanotherendpointsincludingmortality,morbidityand perturbationstoreproduction.Giventhesensitivityofmolecular endpointstoionisingradiationobservedinthispublication,itis imperativethata greaternumberofstudiesfocusonmolecular alterationsinrelationtoeffectsathigherlevelsofbiologicalorgani- sationtoconfirmthesefindingswithinthecrustaceansubphylum.

3. RadiationimpactsonmorbidityinCrustaceans

Morbiditycanbebroadlydefinedas“Alossoffunctionalcapac- itiesgenerallymanifestedasreducedfitness,whichmayrender organismslesscompetitiveandmoresusceptibletootherstressors, thusreducingtheirlifespan”(Copplestoneetal.,2008).Definition ofthetermmorbidityvariesbetweenauthorsandencompassesa vastnumberofendpointsincludingperturbationstogrowthrates, behaviouralalterationsandimmunesystemeffects(Copplestone etal.,2004).Inordertomaintainrelevancebothecologicallyand forenvironmentalprotection,anendpointshouldbeamenableto

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N.Fulleretal./AquaticToxicology167(2015)55–6759 Table2

Numericalbenchmarkvaluesin␮Gy/hr−1proposedbyanumberofdifferentorganisationsanddirectivesfortheprotectionofpopulationsofarangeofbiota.USDOE=UnitedStatesDepartmentofEnergy.NCRP=NationalCouncil onRadiationProtectionandMeasurements.IAEA=InternationalAtomicEnergyAgency.-=Nodataprovided.AdaptedfromAnderssonetal.,(2008).

DoseLevel(␮Gy/h−1)

USDOE(1990) NCRP(1990) IAEA(1992) Environment Canada(2003)

FASSET(2003) Larsson,(2004)

ERICA(2007) Beresfordetal.

(2007)

ICRP(2008) UNSCEAR(2008) PROTECT(2009) Andersson,(2008)

FreshwaterOrganisms 400 400 400 100 10 400 10

Algae 100

Macrophytes 100

BenthicInvertebrates 200

Fish 20

ReferenceTrout 40–400

ReferenceFrog 4–40

MarineOrganisms 400 400 100 10 400

MarineMammals

DeepOceanOrganisms 1000 10

ReferenceCrab 400–4000

ReferenceFlatfish 40–400

ReferenceBrownSeaweed 40–400

TerrestrialOrganisms 100 100 10 100 10

Plants 400

ReferencePineTree 4–40

ReferenceWildGrass 40–400

Animals 40

Invertebrates 200

ReferenceBee 400–4000

ReferenceEarthworm 400–4000

Mammals 100

ReferenceDeer 4–40

ReferenceRat 4–40

Birds 4–40

ReferenceDuck 4–40

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Table3

SummaryofmorbiditystudiesinCrustacea.HTOrepresentsTritiatedWater.Acuteexposuresaredefinedhereasthoselastinglessthan24h,withchronicexposureslasting overaperiodoftheorganismslifespanandgreaterthan24h

Species DoseRate/Total Dose

LowestObserved EffectDose/Dose Rate(LOEDR)

RadiationSource ExposureDuration ExposureType Conclusion Reference

Pollicipespolymerus7.9,62.5nGy/hr−1, 0.625,6.25and 62.5␮Gy/hr−1

0.000625mGy/h−1 HTO 32Days Chronic Alteredmoulting

patterns

Abbott&Mix, (1979)

Daphniamagna 0.02,0.11and 0.99mGy/hr−1

0.11mGy/h−1 241Am 23Days Chronic Reductioninbody

mass,Increased respiratorydemand andReductionin offspringfitness

Alonzoetal., (2006)

Daphniamagna 0.3,1.5and 15mGy/hr−1

0.3mGy/h−1 241Am 70Days Chronic Increasedoxygen

consumption, Reductioninbodysize andmassacross generations

Alonzoetal., (2008a)

Artemiasalina 100,200,400and 800Gy

200Gy 6Co ∼30–220Minutes Acute Decreaseinrespiration rate

Angelovic&Engel (1968)

Callinectessapidus 40,80,160,320 and640Gy

40Gy 6Co ∼11–175Minutes Acute Behaviouralchanges;

reductioninirritability, catatonicstateathigh doses

Engel,(1967)

Daphniamagna 0.41,4.2and 31mGy/hr-1

31mGy/hr−1 137Cs 23Days Chronic Decreasein

mass-specific respirationrate, Reductioninoffspring fitness

Gilbinetal.,(2008)

Nephrops norvegicus

0.5and5Gy 0.5Gy 6Co <5Minutes Acute Morphological

aberrations;

deteriorationof cytoplasmand aberrationsin cytoplasmicorganelles

Mothersilletal., (2001)

Daphniamagna 0.007,0.07,0.65, 4.7and 35.4mGy/hr1

4.7mGy/hr−1 137Cs 75Days Chronic Reductionsinbody

lengthandVon Bertalanffygrowthrate

Parisotetal., (2015)

Palaemonetespugio

&Ucapugnax

9.75,19.5,48.75, 97.5,195and 390Gy

9.1Gy 6Co 0–20Minutes Acute Alterationstomoulting

patterns

Rees,(1962)

Pacifastacus leniusculus trowbridgii

2.8,5.6,8.4,11.2 and16.8Gy

5.6Gy X-Ray 1Minute Acute Behaviouralchanges;

detectionand avoidanceofradiation source

Rodriguez&

Kimeldorf(1976)

Macrobrachium rosenbergii

3,30,300and 3000mGy

3mGy 6Co ∼0–10Minutes Acute Behaviouralchanges;

alterationsto swimmingpatterns;

histologicalaberrations tothegill

Stalinetal.(2013a)

Macrobrachium rosenbergii

3,30,300and 3000mGy

3mGy 6Co ∼0–10Minutes Acute Morphological deformations, Decreased hepatosomaticindex

Stalinetal.(2013b)

measurement,specifictothehazardinquestionandappropriate forextrapolationtohigherlevelsofbiologicalorganisation(Ankley etal.,2010;Suter,1990).Thepracticalityofusingmorbidityasan endpointforradiationexposuremaythereforebelimitedduetothe lackofspecificityandmultitudeofeffectsitincludes.Thisisexem- plifiedwithinthecrustaceansubphylum,withadiversearrayof endpoints(SeeTable3forsummary)usedtoassessmorbidity.

3.1. Radiation-inducedimpactsongrowth&respiration

Alonzo et al., (2006, 2008a) investigated the effects of chronic internal exposure to the alpha emitting radionuclide,

241Americium,onthegrowth dynamicsof Daphniamagna. The authorsrecordedasignificantlylowerdrymassandbodylength ofirradiatedspecimensatdosesof∼1.5mGy/hr−1infirstgener- ationorganisms(F0),withsignificantincreasesintheseverityof effectsovergenerations.Forexample,individualsoftheF2genera- tiondisplayeda15%reductionindrymassatdosesof0.3mGy/hr−1

(Alonzo et al., 2008a). A recent study furtherunderpinned the potential of ionisingradiations to perturb growth dynamics in daphnids(Parisotetal.,2015),withreductionsof5and13 %in thegrowth rateof F2generation daphnidsexposed to 4.7 and 35.4mGy/hr−1ofgammaradiation,respectively.Experimentalevi- dencesuggeststhatlargerdaphnidshaveenhanced competitive and resourceexploitation abilityrelative tosmallerindividuals, leadingtoelevatedmortalityin thoseindividuals withreduced competitioncapacity(KreutzerandLampert,1999).Thefinding thatradionuclideexposuremayperturbgrowthdynamicsthere- forehasimportantimplicationsfornaturalcrustaceanpopulation dynamics.

Inthepreviousstudy(Alonzoetal.,2008a),oxygenconsump- tionofD.magnawaselevatedabovecontrolsatalldoses,suggesting anincreaseinmetabolicexpenditureinducedbyradiationstress.

Exposureoforganisms tostressorsand adverseconditionsmay resultinreallocationofmetabolicenergytowardsmaintenanceand leadtoreducedenergyinvestmentperoffspring(Baillieuletal.,

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N.Fulleretal./AquaticToxicology167(2015)55–67 61

2005).Thiswasreflected by a reduced resistancetostarvation recordedinneonatesderivedfrom0.02mGy/hr−1 exposedadult daphnids(Alonzoetal.,2006).Itisofnotethatthisdoseratefalls belowthevalueof∼0.4mGy/hr1providedbyanumberoforga- nisationsbelowwhichnodeleteriouspopulationleveleffectsare predictedtooccurinaquaticorganisms(SeeTable2)byanorderof magnitude.Arecentstudy(SarapultsevaandGorski,2013)further suggesteddeleteriousimpactsonneonatesrelatingtometabolic perturbations.Followingparentalexposuretoacutegammadoses of100and1000mGyfromCobalt-60,a∼20%decreaseinthemean lifespanofnon-exposedfirstgenerationD.magnaoffspringwas demonstrated.

Anotherstudyof Daphniamagnaexposed tochronicgamma irradiationfrom137Csreportedcontrastingresultstotheafore- mentioned study (Alonzo et al., 2008a) of decreased oxygen consumptionwithincreasingdose(Gilbinetal.,2008).D.magna receivinggammadoseratesof 31mGy/hr1 displayeda signifi- cantlylowermass-specificrespirationrate,comparedwithdose ratesof0.3,1.5and15mGy/hr1allelicitinganincreaseinrespira- tionratefollowingAmericium-241(analphaemitter)exposurein thestudyofAlonzoetal.,(2008a).Whilstthelownumberofrepli- cates(n=6)recognisedbytheauthorinthestudyofGilbinetal., (2008)maypreventcomparisonacrossstudies,thisunderpinsthe importanceofaccountingfordifferingradiationsourcesandthe correspondingvariabilityinrelativebiologicaleffectiveness(RBE).

ThetermRBEwascoinedin1931(FaillaandHenshaw,1931)to accountforthevariabilityinbiologicaleffectobservedwithdose, doserateandtypeofradiation(Valentin,2003).RBEincreasesas afunctionofLETwithhighlinearenergytransfer(LET)sourcesof radiation,e.g.,alphaemitters,typicallymoreeffectiveateliciting biologicaldamageinexperimentalsystemsthanlowLETradiation, i.e.,gammaandbetaraysreachingamaximumat∼100keV/␮m (HallandHei,2003;UNSCEAR,1996).Thismaybeusedtoaccount forthedifferentresponsesofD.magnainthesetwostudies.

Thevariabilityinbiologicaleffectrelatingtothegivenradiation sourceisexemplifiedbyastudyofmorbidityinthegoosebarnacle, Pollicipespolymerus,whichrecordedalteredmoultingpatternsat extremelylowbetadosesof0.62␮Gy/hr−1(AbbottandMix,1979).

Theradiationsourceemployedinthepreviousstudywastritiated water(HTO),aradionuclidethatisdischargedintogroundwater systemsfromnuclearoperations(Jaeschkeetal.,2011;Jhaetal., 2005).Despitetherelativelylowenergy emissionofbetaparti- clesfromHTO(average betaenergy of5.73±0.03keV(Pillinger et al.,1961), thenature and behaviourof this radiation source withinorganismshasledtosignificantconcernovertheRBEof theradionuclide(Bridges,2008;LittleandLambert,2008).Ithas beendemonstratedthatHTOmaybeirreversiblyincorporatedinto organiccompoundswithinorganisms(TakedaandKasida,1979) andthereforemayproducea biologicaleffectdisparatewithits emissioncharacteristics.Inaddition,theauthorsoftheaforemen- tionedstudyonPollicipespolymerus(AbbotandMix,1979)stated thatcalculateddoseswereexclusiveofbackgroundradiationwhich wasnotquantified.Thishighlightstheimportanceofrobustquan- tificationofreceiveddoseinradiobiologystudies(Pentreath,2009).

3.2. Theeffectsofionisingradiationonthebehaviour&

histopathologyofCrustaceanspecies

Ionisingradiationhasbeendemonstratedtoinducebehavioural changesinanumberofcrustaceanspeciesincludingcrabs(Engel, 1967), prawns (Stalin et al., 2013a) and crayfish (Rodriguez and Kimeldorf, 1976). Alterations to behavioural patterns are fundamental in environmental risk assessments since these perturbationsmayariseasanadaptivemechanismtochroniccon- taminantexposureandhavethepotentialtoalterspecies–species interactions(Dell’Omo,2002).Theavailableliteratureregarding

behaviouralimpactsofradiationinvolvesmostlyacuteexposures tohighdosesofradiation(Engel,1967;RodriguezandKimeldorf, 1976),withthemagnitudeofbehaviouralchangescorrelatingwith doselevels.Forexample,Engel(1967)assessedtheimpactofboth chronic and acuteradiation exposures onthebehaviour of the bluecrab,Callinectessapidus,ahighlyaggressiveandcannibalistic species(Bushmann,1999).AreductioninaggressivenessofCall- inectessapidusspecimenssubjecttosingleacuteirradiationswith

6Codosesfrom40to640Gywasobserved,whilsthigherdoses induceda catatonicstate.Continuousexposurestolowerdoses (0.72,1.64&6.53Gy/d−1)for70daysinducedcessationoffeed- ingandabnormalbehaviouralpatternsdeviatingfromthenormal pugnacious natureofC. sapidus,withtheextentofbehavioural effects relating to dose. Whilst the receiveddose remains sig- nificantly higher than estimates of the highest external doses infreshwatersystemsimmediatelyaftertheChernobylaccident ([4.2–8.3mGy/hr1frombottomsediments]Kryshevetal.,2005), the findingthat prolongedexposures may perturb behavioural patterns has implications for contaminated areas where radia- tionlevels remainelevatedoverlong time scales.Furthermore, limited datasuggestsinduction of behaviouraleffects atlower, environmentallyrelevantdoses.Stalinetal.,(2013a)demonstrated behaviouralchangesincludingalterationstoswimmingpatterns inthegiantfreshwaterprawn,Macrobrachiumrosenbergiiatacute gammadosesof3mGy.

Fewstudieshaveconsideredtheimpactsofionisingradiation onmorphologicalandhistologicalparametersincrustaceans.Stalin etal.,(2013a,b)demonstratedinductionofhistologicalandmor- phologicalaberrationsincludingswollenandnecroticlamellaein the gill,deformations of the uropod, and discolouration of the abdomeninM.rosenbergiioveradoserangeof3–3000mGy(Stalin etal.,2013a),withthemagnitudeofeffectsrelatingtodose.Iwasaki (1973)adoptedahistologicalapproachtoassessgammaradiation- inducedeffectsinoogoniaandoocytesofthebrineshrimp,Artemia salina. A dose-dependent increase in cellulardeformations and thenumber ofpyknoticcells (celldegradationcharacterisedby chromatincondensation)wasrecordedoverahighdoserangeof 250–3000GyfromCobalt-60.Furthermore,Mothersilletal.,(2001) recordedperturbations tocytoplasmicorganellesinhematopoi- etic cultures of Nephrops norvegicus at gamma doses of 0.5Gy.

Deformationsincludedabnormalmitochondrial-roughendoplas- mic reticulum complexes at 0.5Gy, progressing to complete disintegration ofthecellular cytoplasmatdoses of 5Gy. Struc- turalperturbationstothegilllamellaeofcrustaceanshavebeen recorded in response toa number of toxicants (Li et al.,2007;

SaravanaBhavanandGeraldine,2000)andmayultimatelyimpair gillfunctioning(Tamseetal.,1995)leadingtoasphyxia.Future studiesshouldconsiderhistologicalimpactsonthecrustaceangill usingchronic,environmentallyrelevantradiationdosesinorder tocorroboratethisfinding.Adecreaseinthehepatosomaticindex ofM.rosenbergiiwasalsoobservedasaconsequenceofradiation exposure(Stalinetal.,2013b)whichmayprovidefurtherevidence thatradiationelicitsalterationstoenergybudgetssincechangesto theHSImayreflectmobilizationandutilizationofenergyreserves (Sánchez-Pazetal.,2007).

Behaviouralanalysisofcrustaceanspeciesexposedtoionising radiationhasreliedlargelyuponanecdotalvisualobservationsover adefinedtimeperiod(Stalinetal.,2013a).Thisapproachissub- jecttoanumberoflimitationsincludingalackofteststandards (Kaneetal.,2004),alowsensitivitycomparablewithvideo-based behaviouralanalysersandthepotentialfor individualbias.Fur- thermore, the available studies have employed acute radiation exposureswhichmayinducedifferentbehaviouraleffectstoequiv- alentdosesdeliveredoverlongertimescales(Solomonetal.,2009).

Futurestudies shouldcouple chronic,environmentally relevant exposuredurationswithahigh-throughputbehaviouraltracking

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system.Suchsystemsminimisebiasbyprovidingsensitive,reliable recordingsofsmallanimalbehaviourundercontrolledconditions.

4. Theeffectofionisingradiationonreproductionin Crustaceans

Reproductive endpoints are frequently the subject of eco- toxicologicaland environmentalrisk assessments studies since perturbationstoreproductionmayimpactuponthelong-termsur- vivalofaspeciesandhencealterecosystemdynamics(Anderson andWild.,1994;Dallasetal.,2012).Alargenumberofpublica- tionshavefocusedonradiation-inducedeffects onreproductive parametersinaquaticinvertebrates,withthereporteddoselevel atwhichsignificanteffectsoccurvaryingbyatleasttwoorders of magnitude (Harrison and Anderson, 1996). This remarkable variabilityis exemplified withinthecrustaceansubphylum; for exampleAlonzoetal.,(2008a,b) recordedadelayedbroodpro- ductioninD.magnaexposedto15mGy/hr1overa23dayperiod (totaldoseof0.345Gy),however10Gywasneededtoelicitadelay in thereproduction ofthe marinecopepod, Paracyclopinanana (WonandLee,2014).Differencesintheexposureduration,spe- cificradionuclideandendpointemployedprecludedevelopment ofageneralised‘doselimit’forreproductiveeffectsincrustacean species.Oneofthepriorityareasforfutureresearchinradioecol- ogyisassessingtheconsequencesofmultigenerationalradiation exposure.ThiswasidentifiedintheresearchagendaoftheStrat- egyforAlliedRadioecology(STAR)group(Hintonetal.,2013)on thebasisthatexposuresacrossgenerationshavelongbeenafocus inhumanradiobiologyandepidemiologystudies(Dubrovaetal., 2000;Koturbashetal.,2006;Nomura,1988),butcomparatively ignoredinnon-humanbiota.Radiation-inducedperturbationsto reproductiveparameters maybeparticularlyrelevant in multi- generational exposure scenarios, since such perturbations may alterpopulationdynamicsandthesubsequentabilityofoffspring toadapttoenvironmentalstressors(Alonzoetal.,2008b;Lynch, 1989,1992).

Theavailableliteraturewithinthecrustaceansubphylumsug- geststhepresence of effects overmultiple generations (Alonzo et al., 2008a;Plaire et al., 2013; Massarin et al., 2010; Parisot etal.,2015;SarapultsevaandGorski,2013).Alonzoetal.,(2008a) and Massarinet al.,(2010) recordedan increase in themagni- tudeofdeleteriouseffects acrossgenerations inDaphniamagna exposedtochronicalphairradiationandchronicwaterborneura- niumexposure,respectively, withsevereimpactstofitnessand reproductioninindividualsoftheF2 generation.Incontrast,the multigenerationalstudyofParisotetal.,(2015)reportedadegree ofrecoveryinF1generationdaphnidsandareducedradiosensi- tivityrelative totheparentalgenerationacrossboth lethaland sub-lethalendpoints(mortalityandfecundity,respectively).Differ- entialradiosensitivitybetweendevelopmentallifestageshasbeen widelyrecordedwithinthecrustaceansubphylum,demonstrated incopepods(Bardilletal.,1977)andArtemiaspecies(Metallietal., 1961).Theauthors(Parisotetal.,2015)hypothesisedthatacumu- lative radiation dose may be necessary to elicit compensatory mechanisms such as DNA repair, accounting for the differen- tialradiosensitivitybetweengenerations.Studiesofradionuclide exposeddaphnidsusingRAPD–PCRmethodshaveindicatedtrans- missionofDNAdamagefromadultfemaledaphnidstoprogeny acrossgenerations(Parisotetal.,2015;Plaireetal.,2013).Thismay bemediatedbyanepigeneticmechanism,ashasbeenproposed forthetransmissionofeffectsinD.magnaexposedtoarangeof chemicaltoxicants(Vandegehuchteetal.,2010)causingalterations togeneexpressionacrossgenerations.Furthermolecularstudies arenecessarytoelucidatethismechanism.Giventheincreasein magnitudeofreprotoxicandtheassociateddeleteriouseffectson

populationdynamics(Alonzoetal.,2008a,2008b)observedover generations,itisimperativethatfuturestudiescontinuetoadopt amultigenerationalapproachasstudiesderivedfromsinglegen- erationexposuresmayunderestimaterisk(Massarinetal.,2010).

Studieswithinthe crustaceansubphylumareheavilybiased towardfemalereproductivesuccess,withtypicalendpointsinclud- ingproductionofneweggs(WonandLee,2014),hatchabilityof eggs(Iwasaki,1964;Sellarsetal.,2005)eggmass(Alonzoetal., 2006, 2008a) and time of hatching (Gilbin et al., 2008). Com- paratively,radiation-induced effectsonmalefertilityhavebeen ignored.Totheauthor’sknowledgenostudyhasdirectlyrecorded theimpactsofionisingradiationonmalefertility.Spermarecon- sideredsensitivetotheinfluenceofxenobioticstressorsincluding ionisingradiation(Fischbeinetal.,1997;LewisandFord,2012;

Marquesetal.,2014).Thisisattributedtotheirlackofinherent defencesystemssuchasantioxidantenzymesandDNArepaircom- parablewithotherbiologicalsystems(Trappetal.,2014).Anumber ofstudieshaveconfirmedthesensitivityofspermtoanthropogenic radionuclides.FollowingtheChernobylcatastrophe an elevated incidenceofspermmorphologicalabnormalitiesandperturbations tospermatogenesiswasobservedinliquidatorsexposedtodoses ofupto0.25Gy(Cheburakov andCheburakova,1992;Fischbein etal.,1997).Furthermorelaboratorystudiesofplaice,Pleuronectes platessa,have demonstrated thatchronicexposures toenviron- mentallyrelevantlowdosesofgammaradiation(0.24mGy/hr−1) aresufficienttocauseasignificantreductioninspermnumberin theseorganisms(Knowles,1999).Experimentalevidenceinaquatic invertebrateshassuggestedthatreductionsinspermnumbersmay havesubsequenteffectsathigherlevelsofbiologicalorganisation.

Thisisexemplified byDunn etal.,(2006),who recordeda 55%

reductioninthesizeoffreshwateramphipod(Gammarusduebeni) broodsaftermatingwithmalesdisplayingaspermcountreduction of56%(LewisandFord,2012).Couplingtheecologicalrelevance ofperturbationstospermparameterswiththeknownsensitivity ofsperm,itisimperativethatfuturestudieswithintheCrustacea includetheseendpointswithinradiobiologicalstudies.

5. Radiation-inducedmortalityinCrustaceans

Despitetherecenttrendtowardsstudiesusingchronicexpo- suresofsub-lethaldoses,theavailableliteratureofradiationeffects incrustaceansremainsdominatedbymortalitystudies.Thisdata isoftenusedtocalculatelethaldose(LD50)values(Dallasetal., 2012)inordertoderivehierarchiesofradiosensitivityacrosstax- onomic groups (Blaylock et al., 1996; Harrison and Anderson, 1996).LD50valuesaretraditionallyusedinecotoxicologicalstud- iestodeterminetheecologicalrisktospecies(Starketal.,2004) andhavealsobeenemployedinordertodeterminenoobserved effectconcentration(NOEC)values(Garnier-Laplaceetal.,2006) toinformradioprotectionandregulatoryefforts.However,many studieshavehighlightedthegreatersensitivityandecologicalrel- evanceofreproductiveendpointsinradiationstudiescompared withmeasurementsofadultmortality(Garnier-Laplaceetal.,2006;

Jonesetal.,2003;UNSCEAR,2008).Thiswasfurtheremphasised byAlonzoetal.,(2008b)whofoundthatanincreaseinindividual mortalityhadareducedeffectonD.magnapopulationgrowthrel- ativetoperturbationstotworeproductivebiomarkers(SeeFig.3).

Incontrast,Starketal.,(2004)recordedthatwithinsomespecies stress-inducedindividualmortalityhadagreatereffectonintrinsic populationincreasethanperturbationstoreproductivecapacity.

Mortalityhasthepotentialtoaltertheagedistribution,deathrate anddensity ofapopulation(UNSCEAR,2008).Furthermore,the derivationofLD50valuesisnecessarytoelucidateagivenspecies sensitivitytoradiationandtodetermineappropriatedoselevelsto employinlaboratoryradiobiologystudies.Thisservestoreiterate

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N.Fulleretal./AquaticToxicology167(2015)55–67 63

Fig.3.PredicteddelayinpopulationgrowthrelativetogenerationtimeinDaphniamagnapopulationsexposedtoalpharadiationdeterminedusingsinglegenerationmodels.

Theeffectsofincreasedmortality,fecundityreductionsanddelaysinreproductiveprocessesattheendpointlevelaremodelled.ReproducedwithpermissionofAlonzoetal., (2008b).

theimportanceofincludinganumberofendpointsinradioecol- ogystudiesandthatinsomecasesderivationoflethaldosedata remainsrelevant.

Withinthecrustaceansubphylum,thedoseatwhichmortality occursdisplaysremarkablevariability(Dallasetal.,2012).Recent workusingtheharpacticoidcopepodTigriopusjaponicusdemon- stratedtoleranceofexternalgammaradiationdosesofupto600Gy, withmortalityonlyoccurring5daysaftercessationofexposure (Hanetal.,2014).Thisiswithinthesameorderofmagnitudeas somebacteriaandprotozoanspecies,groupsconsideredamongst themostradioresistantorganisms(Copplestoneetal.,2001).Fur- thermore,uponirradiationofdryeggmasses,Iwasakietal.,(1971) demonstratedextremeradioresistanceinArtemiasalinanaupliiof upto2780Gyonedayafterhatching.However,Artemiacystsdis- playremarkableresistancetoarangeofstressors(MacRae,2003) attributedtotheirgreatlyreducedmetabolicanddevelopmental activitypriortohatchingandtherefore arenotconsideredrep- resentativeofothercrustaceanspecies.Conversely,Rees(1962) reporteda30dayLD50of∼15Gyinthegrassshrimp,Palaemon- etes pugiowhichis withintheupperbounds ofradiosensitivity of some mammalian species (Blaylock et al., 1996). There are manyproblemsassociatedwithusinglethaldosedatatocompare radiosensitivityacrossorganisms.Forexample,thereisalackof standardisationofthedurationusedtocalculatelethaldosedata varyingfrom4days(Hanetal.,2014)to40days(Engel,1973)which maygreatlyinfluencethefinalvalue.Forchemicaltoxicants,this parameterhasbeenstandardisedinpublishedguidelinesfortests usingDaphniaspecies(OECD,2004),enablingdirectcomparisons ofLD50valuesacrossstressors.Radiobiologicalstudieswouldben- efitfromadoptingasimilarapproachinordertoaidcomparative ability.

Comparatively,theeffectsofchronicradiationdosesonmor- talityincrustaceanshavebeenunderrepresented.Marshall(1966) exposed25populationsofDaphniapulextoexternalgammaradia- tionovera55weekperiodfor18.5hadaywithdosesrangingfrom 0to∼5.1Gy/d−1.Atthethree highestdoselevels(∼5.1Gy/d−1,

∼4.8Gy/d1 and∼4.36Gy/d1)populationscrashedandbecame extinct,whichtheauthorattributedtoanincreaseinindividual deathrateapproachingtheupper limitof thesustainablebirth rate.Othermonitoredparameters suchasthe% ofaborted eggs andembryoswereshowntoincreaseatdoselevelsbelowthose leadingtoextinction,reiteratingthegreatersensitivityofrepro- ductiveendpointscomparabletomortality.Parisotetal.,(2015) corroboratedthesefindings,reportingaslightbutnon-statistically significantincreaseinmortalityin137CsexposedD.magnaatadose

rateof35.4mGy/h1,withsub-lethalimpactsoccurringatmuch lowerdoseratesof0.007mGyh−1.Engel(1967)exposedbluecrabs, Callinectessapidus,toacutedoses(maxiumof180minexposure)of gammaradiationfrom6Cooveratotaldoserangeof40–640Gy atadoserateof219Gy/hr−1.Theauthoralsocontinuallyexposed C.sapidustodoseratesof0.032,0.073and0.29Gy/hr−1overa70 dayperiod.Followingacuteexposurea30-dayLD50of510Gywas recorded.Incontrast,crabssubjectedtoatotalaccumulateddose of∼460Gyatthedoserateof0.29Gy/h−1 overa70dayperiod displayed100% mortality.Althoughthedifferencein total dose precludesusefulcomparison,thegreatersensitivityofC.sapidus followingcontinuousexposureunderpinstheimportanceofthe exposuredurationindeterminingbiologicalimpactinradiobiology studies.Doseratehasbeenreportedtobeanimportantfactorin determiningbiologicaleffectsacrossarangeoforganismsinclud- inginsects(Russelletal.,1958),humans(Elmoreetal.,2006)and rodents(Russelletal.,1959).Forexample,Shimadaetal.,(2005) demonstratedadoseratedependencyoftransgenerationalmuta- tionfrequenciesinspermatogonialstemcellsofMedaka,Oryzias latipes.Theauthorsexposedmalemedakatoan80TBq137Cssource atdoseratesof3Gy/minand9500Gy/min,andrecordedalower mutationfrequencyateachtotaldose(1.9,3.2and4.75Gy)inthe 3Gy/mingroup.

6. Conclusions

Despite numerous international directives and decades of researchintothebiological effects ofradiation,significantgaps inourknowledgestillremain.Althoughcurrentresearchtrends indicateanincreaseinthenumberofpublicationsusingenviron- mentallyrelevant radiationsourcesand durations(Dallasetal., 2012), asignificantdisparitybetweenthenumberof acuteand chronicstudiespersists.ThisisexemplifiedwithintheFREDER- ICAradiationeffectsdatabase.Withinthisdatabase,64%ofthedata pointswereobtainedfollowingacuteradiationexposures,with36%

following chronicexposures.Furthermore,theavailable chronic dataisheavilybiasedtowardsfish,mammalsandterrestrialplants withascarcityofdataevidentinthecrustaceansubphylum(See Table1(Copplestoneetal.,2008).Anothermajorlimitationisthe discrepancybetweentheavailabledataforlaboratorytoxicitytests comparablewithfieldstudies.Themajorityoffielddataisheavily biasedtowardssmallmammals(Bakeretal.,1996;Beresfordetal., 2008;Chesseretal.,2000),fish(Dallasetal.,1998;Jonssonetal., 1999; Sugg etal., 1996Jonssonet al., 1999;Sugg et al.,1996), plants (Kovalchuket al., 1998, 2000; Syomovet al., 1992)and

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Fig.4.Summationoftheavailablechroniceffectdatawithinthecrustaceansubphylumacrossfourendpoints;mortality,morbidity,reproductionandmutation.Thelowest observedeffectdoserate(mGy/h−1)isusedonalogarithmicscale.ThebandofdoseratesselectedbytheICRP(2008)DCRLforthereferencecrabisindicatedby.

birds(Bonisoli-Alquatietal.,2010;Galvánetal.,2014;Hermosell etal.,2013).Comparatively,themajorityoffieldstudiesregarding crustaceancommunitiesexposedtoradionuclidesarefocusedon bioaccumulationofradioactivematerials (Marzano etal., 2000) relatingtotrophic transfer,or calculatingestimates ofreceived doses(Murphyetal.,2011;Batlleetal.,2014).

A summary of the available chronic effect data and the corresponding lowest observed effect dose rate (LOEDR) in crustacean species is shown displayed in Fig. 4. From the limited available data, a tentative hierarchy of radiosensi- tivity in the four endpoints can be derived as follows:

mutation>reproduction>morbidity>mortality.Whilstitmustbe reiteratedthatthisisbasedonextremelylimiteddata(twodata pointsformutation,seeFig.4),thismaychallengetheassump- tionthatreproductionisthemostsensitiveendpointofradiation exposureinnon-humanbiota(UNSCEAR,2008).Responsesatthe molecularlevel,i.e.,alterationstogeneexpression,arefrequently recordedtobesensitiveindicatorsoftoxicantexposureacrossa rangeof organisms(See Section2).Although recentcrustacean radiobiology studieshave demonstrated a shift towardsuse of molecularlevelendpoints(SeeSection2(Hanetal.,2014b;Parisot etal.,2015;WonandLee,2014)),theuseof‘ecotoxicogenomics’

(theintegrationofgenomictechniquesinresponsetoenvironmen- taltoxicantexposure(Iguchietal.,2007))hasbeenafocusofstudies ofothertoxicantsIEendocrinedisruptorsforalmostadecade(Seo etal.,2006).Theobservedsensitivityofmutationasanendpoint observedinthispaperhighlightstheneedtoexploittheadventof cheaperandmoreaccessiblemolecularanalysesinordertovali- datetheusefulnessofmutationasanendpointandevaluatethe potentialofthesetechniquesastoolsinenvironmentalradiopro- tectionandradioecology.Itisimportanttonotethatestablishing linkagesbetweengeneexpressionanalysesandendpointsofhigher levelsofbiologicalorganisationsuchasreproduction,survivaland developmentremainsasignificantchallengeinapplyingecotox-

icogenomicstoecologicalriskassessments(Miracleand Ankley, 2005).Furthermore, transcriptional changes do not necessarily elicitabiologicaleffectwithinagivenorganism(Schirmeretal., 2010).Whilstthisapproachoffershugepotential,untilclearexper- imentallinkscanbedrawnbetweenalterationstogeneexpression patterns and effects at higher levels of biological organisation, monitoringendpoints withclearecologicalimplicationssuchas reproduction,developmentandgrowthremainsimportant.

Inconclusion, thisreviewhassummarized theavailablehis- toricandcurrentliteraturepertainingtoradiation-inducedeffects inanecologicallyrelevantandmodelsubphylum.Sucheffectsare observedoverawiderangeofdoseratesandexposuresources, and could conceivably have ecological consequences for biota chronicallyexposedtoelevatedlevelsofradionuclides.Atpresent howeverthereislimitedpopulationleveldataforaquaticorga- nismsinhabitingchronicallycontaminatedareas.Indeed,astudy oftheabundanceanddiversityofmacroinvertebratecommunities ateightChernobylaffectedlakes(Murphyetal.,2011)foundno evidenceofradionuclidecontaminationimpactingtheecological statusofthewaterbody,andrecordedthehighesttaxonrichness atthemostcontaminatedlake(estimatedtotalexternaldosesof 30.7␮Gy/hr).Clearly,furtherstudiesathigherlevelsofbiological organisationarenecessarytoelucidatethepotentialecologicalcon- sequencesoftheeffectsoutlinedinthisreview.Finally,thisreview hashighlightedthepersistentpaucity ofdataacrosscommonly usedendpointsinthecrustaceansubphylumand identifiedkey gapsintheliteraturetoenhanceresearchwithinthefield.These datagapsmustbeaddressedinordertoenhancetheefficacyofthe subphylumCrustaceaasareferencepointfortheoptimisationand developmentofenvironmentalradioprotectionframeworks.

Conflictofinterest

Theauthorsdeclarenoconflictofinterest.

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