ISSN 1067-4136, Russian Journal of Ecology, 2006, Vol. 37, No. 6, pp. 402–407. © Pleiades Publishing, Inc., 2006.Original Russian Text © V.N. Pozolotina, E.V. Antonova, V.S. Bezel’, T.V. Zhuikova, O.A. Severyukhina, 2006, published in Ekologiya, 2006, No. 6, pp. 440–445.

402

Under conditions of increasing anthropogenicimpact on the biosphere, the ecological study of naturalpopulations in technogenic areas in order to assess theways of adaptation of living organisms to differenteffects is of particular interest. Plant cenopopulationsappear to have a certain capacity for adaptation to nat-ural and technogenic factors and respond to a complexenvironmental impact within the limits of this capacity(Bezel’ et al., 2001). The mechanisms of adaptation arediverse, and every cenopopulation living for a long timeunder certain technogenic stress passes through manystages of natural selection and acquires specific fea-tures. In this context, it is of interest to consider specificfeatures of dandelion populations growing for a longtime under conditions of radioactive contamination (thezone of Eastern Ural Radioactive Trace, EURT) orchemical pollution (the impact zone of the NizhniiTagil Metallurgical Plant, NTMP) in order to estimatetheir adaptive potential and reveal possible preadapta-tion to different technogenic factors.

The purpose of this study was to characterize theviability of the seed progeny of dandelion formed in agradient of radiation or chemical load and to assess theadaptive potential of plants from different cenopopula-tions by exposing the seeds to acute

γ

-irradiation andtreatment with heavy metals (HMs). A comprehensiveanalysis of such data would make it possible to estimatethe degrees of universality and specificity in adaptationto different technogenic factors.

MATERIAL AND METHODSThe common dandelion (

Taraxacum officinale

s.l.)is a polymorphic apomictic triploid (

n

= 8) species. Theembryo develops from an unfertilized egg cell via unre-duced parthenogenesis without pseudogamy (Poddub-naya-Arnol’di, 1976; Ermakova, 1990). Seed sampleswere collected by pooling the seeds of 50–70 dandelionplants from plots with different degrees of chemical andradioactive contamination (the buffer and impact popu-lations). The background (control) plot, similar to otherplots in geobotanical characteristics, was beyond thezone of any technogenic impact.

The first zone of research was situated in the regionNizhnii Tagil, a large industrial center of the Urals. Twosampling plots, designated buffer-m and impact-m,were established at different distances from the NTMP.Both plots had moderately podzolic soils with herb–grass communities dominated by weed species. Appar-ently, the corresponding cenopopulations of dandelionhave been exposed to technogenic impact for about40 years. Soil samples for determining the concentra-tions of HMs were taken from the A1 horizon (depthdown to 10 cm). HMs were extracted with 5%

HNO

3

for 24 h. This method allows extraction of the mobilefraction, which is most easily accessible to plants. Theconcentrations of Zn, Cu, Pb, and Cd were measured ina Perkin-Elmer atomic absorption spectrometer.

The gradient of total chemical soil pollution can beexpressed as an index of toxic load, which allows

Pathways of Adaptation of Common Dandelion Cenopopulations to Long-Term Chemical and Radiation Influences

V. N. Pozolotina, E. V. Antonova, V. S. Bezel’, T. V. Zhuikova, and O. A. Severyukhina

Institute of Plant and Animal Ecology, Ural Division, Russian Academy of Sciences, ul. Vos’mogo Marta 202, Yekaterinburg, 620144 Russia

e-mail: selena@ipae.urn.ru

Received December 22, 2005

Abstract

—A comparative study of the seed progeny of dandelions was performed with samples from cenopo-pulations growing for a long time under conditions of radioactive contamination (the zone of the Eastern UralRadioactive Trace, EURT) or chemical pollution (the impact zone of the Nizhnii Tagil Metallurgical Plant,NTMP). The viability of seeds proved to decrease in a similar way along with an increase in technogenic pres-sure, irrespective of its nature. Experiments on acute exposure to heavy metals and

γ

-irradiation made it possibleto reveal the adaptive capacities of the seed progeny from each cenopopulation. The background sample(formed beyond the zone of any impact) was relatively resistant to irradiation and very sensitive to heavy met-als. The cenopopulations from the EURT and NTMP zones manifested nonspecific responses to the effects ofboth habitual and new factors.

DOI:

10.1134/S1067413606060063

Key words

: radioactivity, heavy metals, cenopopulations, dandelion, Eastern Ural Radioactive Trace, resistanceto

γ

-radiation and heavy metals, specificity of adaptive capacities.

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PATHWAYS OF ADAPTATION OF COMMON DANDELION CENOPOPULATIONS 403

reduction of information on the degree of soil pollutionand indicates the factor by which the background levelof pollution with all metals is exceeded:

where

K

i

is the pollution index of the

i

th point,

ë

ji

is theconcentration of the

j

th element at the

i

th point,

ë

jf

isthe concentration of the

j

th element in the backgroundzone, and

n

is the number of elements included in anal-ysis.

The data shown in Table 1 provide evidence for pos-itive correlations between the concentrations of allchemical elements in the pollution gradient (

r

= 0.99

,

p

= 0.012–0.059), except for Cu (

r

= 0.36–0.45

,

p

=0.70–0.76).

The second zone, the Eastern Ural RadioactiveTrace (EURT), appeared in 1957 after the Kyshtymaccident at the Mayak Radiochemical Plant, where atank with radioactive waste exploded and 2

×

10

6

Ci ofradionuclides spread over a vast area (

Conclusions…

,1991). Short-lived radionuclides, which emitted strongradiation, decayed within the first months after the acci-dent. Today,

β

-emitting

90

S

r

is the main contaminant inthe EURT zone. Additional contamination of this zoneoccurred in 1967 as a result of the wind transfer ofradioactive silt and sand from the banks of shallowingLake Karachai, which had been used as a reservoir forradioactive wastes (with

137

Cs

being the main contami-nant). Two test plots were established along the EURTcentral axis, at distances of 13 and 86 km from the epi-center of the explosion, and named impact-r and buffer-r,respectively. Soil samples were taken from the A1 hori-zon to determine

137

Cs

concentrations in a Canberra

γ

-spectrometer and

90

Sr

concentrations by a radiochem-ical method (Pozolotina et al., 2005).

Ki1n---

C ji

C jf

-------,j 1=

n

∑=

As the plagiotropic part of the dandelion is almostlevel with the soil surface, the dose of radiationreceived by a meristem could be calculated by a simplemodel assuming that the growing point is submergedinto a uniformly contaminated soil layer (0–5 cm). Thecontributions of

90

Sr +

90

Y

and

137

Cs

to dose load werecalculated separately. The absorbed dose rate wasdetermined as follows:

M

=

q

1

+

q

2

,

where

q

1

and

q

2

are measured specific activities of eachradionuclide in the surface soil layer, and

L

is theabsorbed dose rate (cGy/s) produced by this radionu-clide within a uniformly contaminated volume at

q

0

=3.7

×

10

4

Bq/g (Gorshkov, 1967).

The results of these calculations (Table 2) show that,taking into account natural background radiation (aver-aging 10

µ

R/h in the Ural Region), the dose rate wasfour times higher in the buffer plot and 240 times higherin the impact plot than in the control plot.

The quality of seed progeny formed under chemicaland radioactive contamination was assessed by deter-mining a standard set of parameters: the number ofplump seeds in the mixture, their germination rate, thesurvival rate of one-month-old seedlings grown in thesoil from the background plot, and the growth rate ofseedlings (estimated from the number of individualswith true leaves and the length of roots). Root lengthwas also used as a measure of intrapopulation variation:in a laboratory experiment, the seeds from each cenop-opulation (

n

= 100–232) were grown in water and theroot was measured in every seedling. To estimate muta-bility, the proportions of seedlings with chlorophyll dis-turbances, root necroses, profound changes in allorgans, abnormal shape of seminal leaves, and distur-bances of heliotropism were determined.

LSr

90Y

90+( )

LCs

137( )

Table 1.

Concentrations of heavy metals in soils in the zone of NTMP

PlotMetal concentrations,

µ

g/g

K

i

Cu Zn Pb Cd

Background 12.3

±

1.8 19.4

±

3.4 7.9

±

2.3 0.05

±

0.04 1.0

Buffer-m 151.5

±

30.1 152.7

±

17.5 49.6

±

14.4 0.4

±

0.05 8.4

Impact-m 113.2

±

44.8 901.7

±

109.7 193.9

±

18.3 2.7

±

1.1 33.0

Table 2.

Concentrations of

90

Sr and

137

Cs in the surface soil layer (0–5 cm) in the zone of EURT and resulting dose loads ondandelion meristems

PlotConcentration, Bq/kg Dose rate,

n

×

10

–2

µ

Gy/hAnnual dose,

n

×

10

–2

mGy

90

Sr

137

Cs

Background 15 31 1.6 14.0

Buffer-r 646 314 31.8 278.7

Impact-r 80170 4437 2752.0 24116.0

404

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POZOLOTINA et al.

Resistance of the seed progeny to additional effectsof HMs was studied in the experiment with the seedsfrom all samples germinating in contaminated soil fromthe impact plot. Radiosensitivity of seeds from all cen-

opopulations was determined by exposing them to

γ

-radiation from a

60

Co source at a dose of 250 Gy (doserate 41.1 Gy/s). This dose was chosen with regard to thedose–effect curve obtained in a preliminary experi-ment. All experimental data were processed statisti-cally using the STATISTICA for Windows programpackage.

RESULTS AND DISCUSSION

Viability of seed progeny from dandelionsformed in a gradient of radiation or chemical load.

The results demonstrated that the proportions of plumpseeds in all samples were large and practically equal.However, the seed progeny formed in impact zones ofboth factors were inferior to the background progenywith respect to germination rate and the rates of seed-ling survival and growth (Table 3). Analysis of varianceand the faction comparison method confirmed the sig-nificance of differences in all these parameters (

p

<0.05). It should be noted that the degrees of impairmentof seed viability along the load gradient in the NTMPand EURT zones were very similar.

In addition to the average root length, each cenopo-pulation is also characterized by a certain frequencydistribution of this character. An analysis of our data(absolute values were converted into square roots)showed that even the background sample was heteroge-neous, although the pattern of root length distribution init was closest to the Gaussian distribution (Fig. 1). Theroot length distributions in impact samples were char-acterized by left asymmetry with well-manifested cur-tosis, especially in the impact EURT population (curto-sis coefficient 8.4). The distributions in buffer samplesusually had a bimodal shape, providing evidence forheterogeneity of the cenopopulations.

On the basis of these data, seedlings from each cen-opopulation were conventionally divided into twogroups: one with roots shorter than 4.5 arbitrary unitsand the other with longer roots (Fig. 1). The back-ground cenopopulation had 71% of seedlings withshort roots. The proportion of such seedlings in thebuffer plot polluted with HMs increased to 92%,whereas that in the radioactively contaminated bufferplot remained close to the background value (74%).The proportions of short-rooted seedlings in the impact

Table 3.

Viability parameters of seed progenies of the common dandelion from zones of radioactive and chemical pollution

Parameter BackgroundEURT Nizhnii Tagil

buffer impact buffer impact

Proportion of plump seeds, % 87.2

±

7.4 87.6

±

6.3 77.6

±

15.0 89.6

±

8.2 88.6

±

13.0

Germination rate, % 84.0

±

8.0 78.7

± 13.1 50.7 ± 9.5 77.3 ± 12.5 57.3 ± 6.1

Survival rate, % 84.0 ± 7.5 78.7 ± 6.3 50.7 ± 12.4 76.0 ± 10.4 53.3 ± 7.8

Leaf formation, % 67.9 ± 5.8 68.6 ± 7.8 44.2 ± 8.1 61.4 ± 9.2 41.6 ± 6.4

Root length, mm 17.2 ± 1.9 20.8 ± 6.6 13.5 ± 3.7 18.9 ± 9.0 14.8 ± 0.5

1.5 2.5 3.5 4.5 5.5 6.5 7.5

25

20

15

10

5

070

60

50

40

30

20

10

070

60

50

40

30

20

10

0

Root length, mm1/2

Distribution, %

1: d = 0.082, p > 0.20

1

2‡: d = 0.099, p < 0.10; 2b: d = 0.137, p < 0.01

2‡

2b

3‡: d = 0.239, p < 0.01; 3b: d = 0.176, p < 0.01

3‡

3b

Fig. 1. Root length distribution in dandelion seedlings from(1) background, (2‡) buffer EURT, (2b) buffer NTMP,(3a) impact EURT, and (3b) impact NTMP cenopopula-tions (results of the Kolmogorov–Smirnov test for normaldistribution).

RUSSIAN JOURNAL OF ECOLOGY Vol. 37 No. 6 2006

PATHWAYS OF ADAPTATION OF COMMON DANDELION CENOPOPULATIONS 405

plots were even greater: 93 and 85% in the EURT andNTMP zones, respectively. Thus, seedlings of the sec-ond group proved to decrease in number and eventuallydisappear with an increase in toxic load. This parameterreflects the degree of suppression of the seed progenyin cenopopulations. Estimating the state of the cenopo-pulation by the root test, we may represent the gradientof toxic load as the following ascending series: back-ground cenopopulation < buffer EURT plot < impactNTMP plot < buffer NTMP plot = impact EURT cen-opopulation.

Special attention was devoted to seedlings withdevelopmental disturbances. It was found that the fre-quency of root necrosis in the progeny from the bufferand impact zones was increased by a factor of 1.5–2,with root growth in a certain proportion of such plantsbeing restored via the formation of branch roots(Fig. 2A). Seedlings from the impact EURT zoneincluded a large proportion of individuals with pro-found transformation of all organs such as in gnommutants (35% vs. 2.4% in seedlings from the back-ground plot). The disturbances of geo- and heliotro-pism were more often observed in seedlings from thezone of chemical pollution (6.7 and 7.5% in the bufferand impact zones respectively, compared to 3.4% inseedlings from the background plot).

Additional effects of heavy metals and g-radia-tion on seeds. It is expedient to consider our resultsfrom two aspects: first, to analyze the responses ofplants from technogenic zones to additional exposure tohabitual and new factors and compare them with theresponses of the background sample, and, second, tocompare the effects of additional acute exposure tothese factors with the internal control, i.e., with a sam-ple from the same cenopopulation that was not sub-jected to additional stress. These data can provide aclear idea of the adaptation potential of seed progeny inevery cenopopulation.

The additional effect of HMs on seedlings from thebackground cenopopulation proved to be very strong.

The seed germination rate was high, but only 9.3% ofseedlings in this sample survived for one month, withall of them suffering from root necrosis and completelylacking true leaves (Fig. 3). Additional irradiation ofseeds from the background sample had virtually noeffect on their germination rate and the survival of seed-lings. Root growth was strongly retarded, but necrosisoccurred rarely. About 27% of seedlings had trueleaves, i.e., were capable of further development.Therefore, the seed progeny from the background cen-opopulation responded differently to different factors.

The responses of buffer cenopopulations from theEURT and NTMP zones to additional irradiation weresimilar and close to that of the background cenopopu-lation (p � 0.05). However, their responses to addi-tional treatment with HMs differed markedly from theresponse of the background sample (see Fig. 3). Thesurvival and growth rates in both buffer samples werehigher than in the background sample. The parametersof growth in these seedlings significantly decreased incomparison with variants grown in clean soil, but mostsurvivors had true leaves, did not suffer from rootnecrosis, and, therefore, had potential for further devel-opment. An important feature of the buffer cenopopula-tion from the NTMP zone deserves attention: afteradditional treatment with HMs, root necrosis in theseplants developed more frequently than in the impactsample, but 41% of seedlings recovered by formingbranch roots (see Fig. 2B). The formation of branchroots after additional irradiation was rare in seedlingsfrom all cenopopulations (see Fig. 2C).

Impact samples significantly differed from oneanother in the resistance to HM as well as to γ-irradia-tion (Fig. 3). The proportion of seedlings with trueleaves in the impact EURT cenopopulation was close tothat in the buffer zone after both types of additionaltreatment, but virtually no viable seedlings remained inthe NTMP sample after additional treatment.

Thus, seed progeny with decreased parameters ofviability and high mutability is formed in cenopopula-

Relative number of seedlings, %1009080706050403020100

1

2‡

3‡ 2b3b

12‡

3‡2b

3b

1

2‡3‡

2b

3b

A B C

Fig. 2. Numbers of seedlings with root necrosis (whole column) and the proportion of seedlings restoring the root system on accountof branch roots (light part of the column) in the control (A), after additional treatment with heavy metals (B), and after additionalirradiation at a dose of 250 Gy (C). Cenopopulations: (1) background, (2a) buffer-r, (2b) buffer-m, (3a) impact-r, and (3b) impact-m.

406

RUSSIAN JOURNAL OF ECOLOGY Vol. 37 No. 6 2006

POZOLOTINA et al.

tions growing for a long time in areas with different lev-els of chemical or radioactive contamination. Using thesurvival of seedlings as an example (see Table 3), it ispossible to make a mathematical approximation reflect-ing changes in this parameter in a gradient of chemicaland radioactive contamination:

ym = –15.35xm + 101.8, R2 = 0.929;

yr = –16.65xr + 104.43; R2 = 0.866,where ym and yr are the survival rates of seedlings fromthe NTMP and EURT zones, respectively, and xs and xrare the loads accounted for by HMs and radionuclidesin natural populations. The fact that the parameters ofthis equation almost coincide suggests that theresponses of seed progenies have a similar, unspecificcharacter, irrespective of distinguishing features of thefactors and the strength of their action (see Tables 1, 2).Similar trends were also obtained for other parameters.Recall that, compared to the background plot, the radi-ation load in the buffer and impact plots of the EURTzone was 4 and 240 times higher and the chemical loadin the plots of the NTMP zone was 8 and 33 timeshigher, respectively, than in the background plot. Thesefacts agree well with published data. A comparison ofthe ecological effects of different toxic agents showedthat radiation doses causing initial detectable effectsand doses resulting in complete destruction of the sys-tem differed by factors of 15–20, but such a transitionin the case of exposure to HMs was already observedwhen the toxic load increased by a factor of only 2–10(Fuma et al., 2003).

The seeds from the background sample manifestedminimal adaptation to the effect of HMs upon addi-tional exposure, but they proved to be relatively resis-

tant to acute irradiation. This fact indicates that the twofactors differ in the mechanisms of their action on theseed progeny that has not yet been exposed to any tech-nogenic stress. Such an effect was expected, becausedetailed data on the action mechanisms of ionizingradiation and HMs were published previously (Ras-teniya…, 1983; Grodzinskii, 1989; Geras’kin et al.,1996). Concerning the background population used inour study, we may conclude that approximately one-quarter of seeds in a random sample tolerates additionalacute irradiation, but there are no plants capable ofgrowing in soils polluted with HMs.

The adaptive potential of seed progenies from thebuffer cenopopulations, which had been exposed for along time to moderate toxic or radiation stress, wasbasically different from that of the background sample.It is obvious that these progenies contained a relativelylarge proportion of plants resistant to agents of differentnatures. Upon acute exposure, the specificity of factorswas clearly manifested only with respect to the survivalof seedlings: this parameter sharply decreased underthe effect of additional treatment with HMs butremained high for one month after additional irradia-tion. However, this criterion does not fully characterizethe viability of seedlings, because it does not reflect thestate of meristems. The proportion of plants capable offurther development can be determined from growthparameters (leaf formation and root length). However,no specificity of plant responses to habitual and newfactors was revealed by these criteria. It appears that,after the initial effects reflecting specific features of theacting factor, secondary physiological processes deter-mined by characteristics of the plant itself develop inseedlings. We can only note the tendency toward an

%140

120

100

80

60

40

20

0HMs 250 Gy HMs HMs250 Gy HMs250 Gy 250 Gy HMs 250 Gy

background buffer-r buffer-m impact-r impact-m

1 2 3

Fig. 3. Main parameters of viability of dandelion seedlings from different cenopopulations after additional exposure to effects ofheavy metals and γ-radiation (relative to the control without exposure, %): (1) survival of seedlings, (2) number of seedlings withtrue leaf, and (3) root length.

RUSSIAN JOURNAL OF ECOLOGY Vol. 37 No. 6 2006

PATHWAYS OF ADAPTATION OF COMMON DANDELION CENOPOPULATIONS 407

increased resistance to HMs in seeds formed in the zoneof moderate chemical influence (the buffer NTMPzone). Upon repeated treatment with HMs, plantsgrown from these seeds proved to be more capable ofrestoring their root systems after necrosis of the mainroot. There are published data on other species that con-firm the increased resistance to HMs in plants growingin the zones of heavy metal pollution (Alekseeva-Pop-ova, 1990).

A comparison of seed progenies from impact plotsafter additional treatment confirms the nonspecificcharacter of their responses. The sample from theNTMP zone proved to be virtually incapable of resist-ing additional chemical or radiation impact, whereasthe sample from the EURT zone included groups ofplants that survived after exposure to either factor.Therefore, populations growing for a long time inradioactively contaminated areas produce seed progenywith a relatively large proportion of radioresistantseeds, with the proportion of plants resistant to HMsbeing similarly large. No such trend is observed in thebackground population.

CONCLUSIONS

(1) In seed progeny of dandelions from cenopopula-tions with different types and degrees pollution, allparameters of viability proved to decrease in a similarway, with the same deleterious effect being caused byan increase in radiation dose by two orders of magni-tude and an increase in heavy metal concentrations byone order of magnitude.

(2) Assessment of the adaptive capacities of seedprogenies from cenopopulations exposed for a longtime to moderate chemical or radiation stress showedthat their response to the additional impact of habitualand new factors was unspecific. In the background pop-ulation, on the contrary, specificity of responses toeither factor was clearly manifested.

(3) The specific response of seedlings from thebuffer NTMP cenopopulation to the additional impactof HMs, manifested in stimulation of processes leadingto restoration of the root system, may be regarded aspreadaptation to the habitual factor.

ACKNOWLEDGMENTS

This study was supported by the Russian Founda-tion for Basic Research-Urals, project no. 04-04-96099; the Scientific School Support Program, projectNSh-5286.2006.4; a Young Scientists grant no. MK-

4788.2006.4 from the President of the Russian Federa-tion; and the Federal Agency for Education, orderNTGSPA.

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