Nordic Society Oikos
Developmental Instability of Plants and Radiation from Chernobyl
Author(s): Anders Pape Møller
Source: Oikos, Vol. 81, Fasc. 3 (Apr., 1998), pp. 444-448
Published by: Wiley on behalf of Nordic Society Oikos
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OIKOS 81: 444-448.Copenhagen
1998
Developmental
instability
of plantsand radiationfromChernobyl
AndersPape Moller
Moller, A. P. 1998. Developmentalinstabilityof plants and radiationfromChernobyl. - Oikos 81: 444-448.
Phenotypicmeasuresof developmentalinstability
wereused to assess the hypothesis
that radiationfromChernobylin Ukraine directlyaffectsthe developmentalprocesses of plants.Fluctuatingasymmetry
and thefrequencyof phenodeviantsin three
species of plants,Robiniapseudoacacia,Sorbus aucupariaand Matricariaperforate,
were assessed along a transectfromthe securityzone of Chernobyltowards the
largelyuncontaminatedarea 225 km SE of Chernobyl.Measures of developmental
instabilitydecreasedin a similarway for the threespecies withincreasingdistance
fromChernobyl,the level of developmentalinstabilitybeing threeto fourtimesas
largenear Chernobylas in thecontrolarea. Developmentalinstability
was positively
relatedto the level of radiationby caesium-137along the transect.In conclusion,
radiationfromChernobylhas resultedin a reducedabilityof plants to controlthe
stabilityof theirdevelopmentalprocesses.
A. P. Miller, Laboratoired'Ecologie, CNRS URA 258, UniversitW
Pierre et Marie
Curie,Bat. A, 7amestage, 7 quai St. Bernard,Case 237, F-75252 Paris Cedex 05,
France ([email protected]).
Although10 yearshave passed sincetheaccidentat the binismof barnswallowswas considerablyelevatednear
nuclear power plant in Chernobyl,Ukraine,relatively Chernobylcompared to controlareas (Ellegrenet al.
littleis known about the biological consequences of 1997). Deviant morphologicalcharactershave someextensiveradioactivecontaminationof vast areas of timesbeen shown to be associated withselectivecosts
Central and NorthernEurope (Moller 1993, Baker et in terms of mortalityand reduced mating ability
al. 1996, Dubrova et al. 1996). This is surprising
given (Moller 1993, Ellegrenet al. 1997).
that importantbiological knowledgecan be obtained
Developmentalstabilityof organismsprovidesa senconcerningthe consequencesof adverseenvironmental sitivemeasureof the abilityof individualsto undergo
conditions on phenotypicexpression,genetics,selec- stable developmentof repeatedcharactersundergiven
tion, and micro-evolution.Previous studies have environmental
conditions(Parsons 1990a, Moller and
demonstrated
thatnovel gene sequenceshave appeared Swaddle 1997). A range of environmental
and genetic
at a veryhigh frequency(Baker et al. 1996), and that factorsis knownto affecttheabilityof a widevarietyof
mutationsof several genetic systemshave increased organisms to develop stable phenotypes (Parsons
considerablycomparedto controlareas (Dubrova et al. 1990a,Freemanet al. 1993,Graham et al. 1993,Moller
1996, Ellegrenet al. 1997). The frequencyof deviant and Swaddle 1997). Measures of developmentalinstaphenotypeswas considerablyincreasedaround Cher- bility,such as fluctuating
asymmetry
and the frequency
nobylas determined
fromfluctuating
in tail of phenodeviants(Freeman et al. 1993, Graham et al.
asymmetry
lengthof the barn swallow Hirundorustic, but not in 1993, Moller and Swaddle 1997), are oftenmuchmore
othermorphologicalcharacters,havingincreasedby a sensitiveindicatorsof currentenvironmental
conditions
factorthreeto fourcomparedto nearbycontrolareas than traditionalmeasuresused formonitoringsuch as
(Moller 1993). Similarly,the frequencyof partial al- various fitnesscomponentslike growth,fecundityand
Accepted 12 September1997
Copyright?) OIKOS 1998
ISSN 0030-1299
Printedin Ireland - all rightsreserved
444
OIKOS 81:3 (1998)
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survival(Moller and Swaddle 1997),and developmental
instability
can be assessed well beforethe environmental conditionactually has resultedin a reductionin
fitness(Clarke and McKenzie 1992, Graham et al.
1993, Moller and Swaddle 1997).
The aims of thisstudywereto determine
therelationship between the level of fluctuatingasymmetryin
plants and radiationoriginatingfromChernobyl.This
was done by monitoringthe level of phenotypicdeviance in threeplant species along a transectfromnear
the securityzone of the Chernobylarea to a control
area in SE Ukraine.I testedforconsistency
in estimates
of developmentalinstabilityacross plant species by
determining
consistencyin the rank of developmental
instability
along the transect.Finally,I determinedthe
relationshipbetweenestimatesof developmentalinstabilityand radiationfromcaesium-137along the transect.
branches pointing towards west. A total of 26 000
leaves from260 treeswereinvestigated.
Camomileis an
annual composite with radially symmetricalflowers.
Fluctuatingasymmetry
of petals was calculatedas the
mean difference
betweenthe lengthof the shortestand
the longestpetal of two flowerheads fromeach of 20
randomlychosen plants. A total of 520 flowersfrom
260 plants was investigated.Damaged and withered
leaves or flowerswere not measured. Damage was
assessed fromcharactersbeingpartiallymissingor destroyed.It is unlikelythat this exclusioncaused any
bias in the resultssince less than 3%Sof all
significant
leaves/flowers
were damaged or withered.
Characters demonstratefluctuatingasymmetryif
signed left-minus-right
charactervalues are normally
distributedwitha mean value of zero. Leaf and petal
was fluctuating
as demonstrated
asymmetry
asymmetry
by signed left-minus-right
charactervalues being normallydistributedwitha mean value not deviatingsignificantlyfromzero (Lilliefors'tests and one-sample
t-tests,P > 0.20). Measurementerrorsof signedasymmetriesand the proportionof malformedleaves were
Materialsand methods
assessed fromone-wayanalysesof variance(Yezerinac
During June 1996 I monitoredfluctuating
asymmetry et al. 1992), and theywere always lower than 5%YO
as
and the frequencyof phenodeviantsof threecommon determinedfromrepeatedmeasurements
of all characplant species, black locust tree Robinia pseudoacacia, terson a sample of 10 plantson two subsequentdays.
rowan Sorbusaucuparia,and camomileMatricariaperforata, along a gradientfromthe securityzone of the
Chernobylarea towards southeast of Kiev; an area
unaffected
by radioactivecontaminationdue to prevailResults
ing southerlyand south-easterly
windsduringthe first
stage of the accident.The level of radiationalong this All threespecies demonstratedlevels of developmental
gradientafter the accident in April 1986 decreased instabilitynear the securityzone threeto four times
markedlyfromjust outsidethe southernborderof the larger than in uncontaminatedareas away from the
securityzone to Kiev (114 km SE of Chernobyl). Chernobylarea (Fig. 1). These differences
in developMeasurementsof radiationfromsoil samplescollected mentalinstabilityamong studyareas were statistically
by the Ukrainian Ministryof Health and Medicine significant(Kruskal-Wallisone-way analysis of varifromnine sites along this gradientin 1991-1994 re- ance, P < 0.001 in all threecases).
vealed levels of radiation from caesium-137 ranging
The threeplantspeciesdemonstrated
similarpatterns
from 1.10 to 4.66 Ci/km2with relativelystable levels of developmentalinstabilityfromhigh levels near the
duringthe period of investigation.
securityzone with a subsequent marked drop to a
Black locust treeshave pennateleaves withthreeto constantlow levelnear Kiev and further
away fromthe
ten directlyopposed leaflets and a single terminal Chernobylarea (Fig. 1). This patternof covariationin
leaflet.Fluctuatingasymmetry
of leaves was calculated developmentalinstabilitywas highlyconsistentamong
as the mean distancemeasuredwith a calliperto the specieswithspeciesshowingsimilarpatternsof deviant
nearest mm between opposing leafletsof five leaves morphology,as determined
froma Kendall's coefficient
fromeach of 20 randomlychosen treesof a heightof of concordance (W= 0.97, x2= 34.72, df= 2, P <
1-5 m. Leaves were chosen froman apical position 0.001). A commoncause of the elevatedlevel of develinwardsat a heightof 1-2 m frombranchespointing opmentalinstability
is therefore
likelyin thethreeplant
towardswest.A totalof 1300 leaves from260 treeswas species.
measured.Rowan has pennateleaves witha numberof
The correlationbetween phenotypicdeviance and
pairs of opposed leaves and a single terminalleaflet. level of radiationfromcaesium-137was assessedforall
For rowan developmentalinstabilityof leaves was cal- threeplant species. There were stronglypositiverelaculated as the proportionof 100 leaves without a tionshipsforall threespecies,witha fourfoldincrease
terminalleafletfromeach of 20 randomlychosen trees in developmentalinstabilitybeing associated with a
of a heightof 1-5 m. Again, leaves were chosen from fivefoldincrease in radiation (Fig. 2; Robinia: F=
an apical positioninwardsat a heightof 1-2 m from 35.24, df=1,11, r2=0.76, P<0.0001; Sorbus: F=
445
OIKOS 81:3 (1998)
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Fig. 1. Developmental
instabilityof threespecies of
plantsin relationto distance
fromthe Chernobylpower
plant. Developmental
instabilityis estimatedas
5
Robinia
* Sorbus
0
absolute fluctuating
(mm) for Robinia
asymmetry
and Matricariaand the
percentageof phenodeviant
leaves (x 0.1) forSorbus.
Values are means (SE).
Matricaria
.*n
>%
T
.I
X
0.
2 -
0)
1
0'.
0
I
100
.
I
200
I
300
Distance(km)
206.84, df= 1,11, r2= 0.95, P <0.0001; Matricaria:
F=35.81, df= 1,11, r2=0.77, P<0.0001). This finding is consistentwith radiationbeing associated with
variationin developmentalinstabilityof plants among
sites.
Discussion
Threeplant speciesdemonstrated
consistentpatternsin
deviantphenotypesbeing associated with the distance
fromthe Chernobylpowerplant(Fig. 1), and radiation
from radioactive contaminationmay constitutethe
causal factor,sincemeasuresof developmentalinstabilitywerestronglypositivelyrelatedto the levelof radiation by caesium-137(Fig. 2). Obviously,whetherthis
correlationalrelationshipis causal can only be demonstratedby experiments.The level of phenotypicdeviance near the securityzone was three to four times
largerthanin thecontrolarea. Interestingly,
fluctuating
asymmetryin length of tail feathersof male barn
swallows investigatedduring a previous study in
Ukrainewas also approximately
fourtimesas large as
in an uncontaminatedcontrolarea in Ukraine,and as
in the contaminatedarea beforethe accident (Moller
1993). The effectsof low levelsof radiationhave previously successfullybeen assessed from developmental
instabilityof plants and animals (Bagchi and Iyama
1983,Parsons 1990b). The presentstudysuggestedthat
the biological consequences of even small levels of
radiationreadilycan be assessedfromfluctuating
asymmetryand the frequencyof phenodeviants.
The magnitudeof the effectsof radioactivecontamination on developmentalinstabilityfromthe present
studycan be comparedto otherstudiesusingdifferent
kindsof environmental
stressors.For example,a recent
fortwo spestudyusing extremerearingtemperatures
cies of fruitfliesdemonstratedincreasesin asymmetry
by a factortwo to threeforthreedifferent
morphological characters(Imashevaet al. 1997). A studyusingfin
in grunionLeuresthestennisdeveloping
ray asymmetry
under differentlevels of DDT concentrationin sea
water demonstratedan increase in asymmetryby a
factor five (Valentine and Soul& 1973). Many other
examplesbased on otherstressorsin otherspecieshave
demonstratedeffectsof a similarmagnitude(reviewin
Moller and Swaddle 1997).
The causes of developmentalinstabilityare both of
environmental
and geneticorigin,and previousstudies
have shownthatradioactivecontaminationfromChernobylhas resultedin geneticchanges(Baker et al. 1996,
Dubrova et al. 1996,Ellegrenet al. 1997) thatmayhave
been the directcause of increaseddevelopmentalinstability.Mutationshave caused increasesin developmental instabilityin a numberof different
organisms,and
the effectsof mutationson developmentalperformance
often resemblethose of mutationsper se (review in
Moller and Swaddle 1997). The fitnessconsequencesof
asymmetric
phenotypesremainunknownin the present
study,but elevated levels of asymmetry
and irregular
446
OIKOS 81:3 (1998)
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Fig. 2. Developmental
of threespecies of
instability
plantsin relationto
radiationfromCS137
(Ci/km2)fromthe
Chernobylpower plant.
is
Developmentalinstability
estimatedas absolute
(mm)
asymmetry
fluctuating
for Robiniaand Matricaria
50
*
4-
x
.
of
and thepercentage
Matricaria
H
3
phenodeviantleaves ( x 0.1)
forSorbus. Values are
means (SE).
Robinia
Sorbus
2
a)~
~~2
0~~~~~0
Ih
10
1
Radiation (Cisq.
phenotypeshave been associated with reductionsin
and
fitnesscomponentsrangingfromgrowth,fecundity
survivalto matingsuccess in a wide varietyof plants
and animals (Moller 1997, Moller and Swaddle 1997).
Selectionoftenacts againstindividualswithdevelopmentallyunstable phenotypes(review in Moller and
Swaddle 1997), and a large number of studies has
how survivalprospectsand longevityare
demonstrated
phenotypes(reviewin Moller
associatedwithsymmetric
1997). The resultsreportedin thepresentstudyare thus
the real effectof radiationon
likelyto underestimate
developmentalinstability,since individuals with the
mostasymmetric
and aberrantphenotypesare likelyto
have been under-representedbecause of selective
weresimilarforthe
deaths.The patternsof asymmetry
singleannual and thetwo perennialplantspecies.Selectionagainstasymmetric
phenotypesis likelyto be more
importantin perennials,whereselectionmayhave acted
of theresultsfor
duringseveralyears,and thesimilarity
all threespecies suggeststhat it is unlikelythat past
selectionepisodes have seriouslybiased the findings.
In conclusion,threespecies of plants demonstrated
consistentassociations between distance from Chernobyl and measuresof developmentalinstability,and
therewas a stronglypositiverelationshipbetweenradiation fromcaesium-137and developmentalinstability.
km)
References
Bagchi,S. K. and Iyama,S. 1983. Radiation induceddevelopmentalinstabilityin Arabidopsisthaliana.- Theor. Appl.
Genet. 65: 85-92.
Baker,R. J.,Van Den Bussche,R. A., Wright,A. J.,Wiggins,
L. E., Hamilton,M. J., Reat, E. P., Smith,M. H., Lomakin, M. D. and Chesser, R. K. 1996. High levels of
geneticchange in rodentsof Chernobyl.- Nature 380:
707-708.
Clarke,G. M. and McKenzie, L. J. 1992. Fluctuatingasymmetryas a quality controlindicatorfor insectmass rearing
processes.- J. Econ. Entomol. 85: 2040-2050.
Dubrova, Yu. E., Nesterov, V. N., Krouchinsky,N. G.,
Ostapenko,V. A., Neumann,R., Neil, D. L. and Jeffreys,
A. J. 1996. Human minisatellitemutationrate afterthe
Chernobylaccident.- Nature 380: 683-686.
Ellegren,H., Lindgren,G., Primmer,C. R. and Moller,A. P.
1997. Fitnessloss and germlinemutationsin barn swallows
breedingin Chernobyl.- Nature 389: 593-596.
Freeman, D. C., Graham, J. H. and Emlen, J. M. 1993.
stress,and
Developmentalstabilityin plants: symmetries,
epigenesis.- Genetica 89: 97-119.
Graham, J. H., Freeman, D. C. and Emlen, J. M. 1993.
Developmentalstability:a sensitiveindicatorof populations understress.- In: Landis, W. G., Hughes,J. S. and
Lewis, M. A. (eds), Environmentaltoxicologyand risk
assessment.AmericanSociety for Testing and Materials.
ASTM STP 1179, Philadelphia,PA, pp. 136-158.
Imasheva, A. G., Loeschcke, V., Zhivotovsky,L. A. and
on
Lazebny, 0. E. 1997. Effectsof extremetemperatures
phenotypic variation and developmental stability in
and DrosophilabuI:atii. - Biol. J.
Drosophilamelanogaster
Linn. Soc. 61: 117-126.
- I am grateful
to A. A. Tokarforhelp
Acknowledgements
withthefieldwork.P. A. Parsonsand L. Svenssonprovided Moller, A. P. 1993. Morphologyand sexual selectionin the
barn swallow Hirundorustic in Chernobyl,Ukraine. by grants
constructive
criticism.
The research
was supported
fromtheDanishNaturalScienceResearchCouncil.
Proc. R. Soc. Lond. B 252: 51-57.
447
OIKOS 81:3 (1998)
This content downloaded from 128.39.236.139 on Fri, 28 Jun 2013 01:47:11 AM
All use subject to JSTOR Terms and Conditions
- 1997. Developmentalstabilityand fitness:a review.- Am.
(ed.), Evolutionarygeneticsof Drosophila.Plenum Press,
Nat. 149: 916-932.
New York, pp. 75-86.
- and Swaddle,J. P. 1997.Asymmetry,
developmentalstabil- Valentine,D. W. and Soul, M. 1973. Effectof p,p'-DDT on
ityand evolution.- OxfordUniv. Press,Oxford.
developmentalstabilityof pectoralfinraysin the grunion,
Parsons, P. A. 1990a. Fluctuatingasymmetry:
an epigenetic
Leuresthestennis.- Fish. Bull. 71: 921-926.
measureof stress.- Biol. Rev. 65: 131-145.
Yezerinac, S. M., Lougheed, S. C. and Handford,P. 1992.
- 1990b. Extreme environmental stress: Asymmetry,
Measurementerrorand morphometricstudies: statistical
metabolic cost and conservation.- In: Barker,J. S. F.
powerand observerexperience.- Syst.Zool. 41: 471-482.
448
OIKOS 81:3 (1998)
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