michaux—biology of cirsium vulgare

New Zealand Journal of Botany, 1989, Vol. 27: 401^4140028-825X89/2703-O401-$2.50/0 © Crown Copyright 1989

401

Reproductive and vegetative biology of Cirsium vulgare (Savi) Ten.(Compositae: Cynareae)

B. MICHAUXZoology DepartmentUniversity of AucklandPrivate BagAucklandNew Zealand

Abstract Achenes of Cirsium vulgare germinatedat constant temperatures between 7°C and 32°C.Fresh achenes had a higher optimum temperature ofgermination (23.5°C) than older achenes which hadbeen stored for 10 months (20°C). Fresh achenesalso germinated more slowly and had a lowermaximum level of germination. Achenes that wereburied in the soil showed a decrease in viability overtime. At depths of 2 cm achenes either germinated orwere destroyed. At greater depths theachenes showedan exponential decay rate in viability with time. Theslope of this exponential curve decreased withincreasing depth of burial. Germination in the fieldwas synchronous with rainfall pattern over thesummer, although subsequent germination may occurif achenes are brought to the surface. Young seedlingswere not damaged by frosts of -2°C. Aftergermination a major root system developed rapidly,whilst a rosette more slowly formed above ground.Rosettes increased in diameter until the winter whengrowth ceased, although horizontal growth wasreinitiated if the rosette became damaged. In latewinter or early spring vertical growth is initiated,leading to the formation of a bushy plant withsubsequent flowering and production of achenes. C.vulgare flowers throughout the spring and summerwith the maximum number of plants flowering in thelate spring or early summer. Each capitulum holdsapproximately 200 achenes and a large plant mayproduce in excess of 50,000 fertile achenes. Apartfrom fertile achenes, "shrunken" and "hollow"

Received 23 May 1988; accepted 31 January 1989

achenes are also produced by non-pollination andself-pollination respectively. After the capitulumhas matured the achenes are wind dispersed.However, despite the presence of a pappus themajority of achenes fall within a circle of radius 1.5times the height of the parent plant. In conjunctionwith the production of non-viable achenes throughself-fertilisation, this is expected to result in marginalspread of this species from existing infestations.

Keywords Cirsium vulgare; weeds; seed biology;vegetative growth; reproductive biology; winddispersal; biological control

INTRODUCTION

Cirsium vulgare (bull or spear thistle, known asScotch thistle in New Zealand) is a biennial herb,typically 50-150 cm in height, that occurs throughoutNew Zealand in disturbed habitats and pasture. Thisthistle was introduced from Europe in the latter halfof last century, probably as a contaminant of grass orcereal seeds. Two chromosome races have beenrecorded from Europe (Tutin et al. 1976) with In =68 and 102 respectively. Local populations sampledby Michaux (1984) had a diploid chromosomenumber of 68.

Cirsium vulgare reproduces entirely throughachenes, henceforth referred to as seeds. Disc floretsare contained within a capitulum, which itself iscomposed of numerous simple bracts that have long,sharp apical spines. The seeds are held upon areceptacle and are surrounded by setae which developfrom the receptacle surface (Fig. 1 A). The pappus isattached to the achene along a disc-like structure.

The stamens are situated near the base of thetubular corolla (Figs. IB and ID). There are fivestamens from which free filaments emerge,eventually fusing to form an anther tube. The styleenters the anther tube at the base. When the floret hasmatured the style breaks through the end of theanther tube carrying with it pollen that has adheredto it (Fig. 1C). The pollen is stored in the anther tube.

402 New Zealand Journal of Botany, 1989, Vol. 27

Fig. 1 A transverse section through a capitulum. B asingle floret with detail of stamen positions. C detail ofstigmatic lobe and adhered pollen. D transverse sectionthrough a corolla.

Mechanical stimulation, such as produced bypollinating insects, causes the style to extend further.This extension continues until the style is straight.Following this the stigmatic lobes open and thestigma is ready to receive pollen. Florets do notmature synchronously, the outer florets maturingfirst and the innermost last. This is probably areflection of the order in which the florets develop,presumably a reflection of the phyllotaxis of flowerdevelopment

The number of flower heads on a plant iscorrelated to its overall size, as measured by theplant's maximum diameter as a rosette (y = 4.4x -152; i^= 0.81; y = flower numbers; x = maximumrosette diameter [cm]). The flower heads are eithersingle or in groups of three, situated at the apex of thenumerous branches of the inflorescence (terminalflower heads), or growing at the apex of lateral stems

(lateral flower heads). The corolla is a light purplecolour and the filament tube somewhat darker.Individual flower heads last for only a few daysbefore the floral tissue wilts, the involucre bractsthen turn brown and open out (the time takendepending on the humidity) exposing the pappus tothe air. The innermost seeds are dispersed first as thereceptacle arches upwards due to the opening of thebracts (Small 1918). The pappus attached to themthen becomes subject to air movement. A singleplant may remain in a flowering state anywhere fromone to six weeks depending on the number of flowerson it. Pollinators include the honey bee (Apismellifera), bumblebees (Bombus spp.), and hoverflies(Diptera: Syrphidae), although various adultLepidoptera, Thysanoptera, and Hymenoptera(Leioproctus spp.) may also act as pollinators.

This study was carried out as part of aninvestigation into the feasibility of controlling C.vulgare through an integrated approach involvingsuch factors as pasture management and theintroduction of biological control agents. In order toimplement such an approach considerable detail ofthe biology of the target weed has to be known. Theoverwhelming preponderance of papers in theliterature concern biochemical responses of weedspecies. In comparison there are few that focus ongeneral biology - an indication of the type of datarequired when herbicidal control is thedesired option.Traditionally this type of control has been the onlyoption, yet for a variety of reasons other controlstrategies are now being explored and in some casesimplemented. Because these alternative methodsrequire a knowledge of why the weed is a problembefore a solution can be found to control it, details ofmany aspects of the weed's biology need to beknown. It is this information for C. vulgare that isreported in this paper.

SAMPLE SITES AND MATERIALS

Two study sites were used at Kaukapakapa which is40 km north-west of Auckland (36°35'S 174°25'E).Kaukapakapa is situated in a broad river valley. Thesoil is predominantly a heavy clay loam, althoughsome restricted areas of alluvial silt are also found.The climate is typical of much of Northland, withannual rainfall in excess of 1000 mm and a meantemperature of 16°C. The winters are wet and thevalley soils are frequently saturated. In summerthese soils are subject to extensive drying causingretardation of pasture growth and the development

Michaux—Biology of Cirsium vulgare 403

of deep cracks, particularly so on the clay soils.Despite thisarea'sproximity to theKaipara harbour,heavy frosts are experienced during the winter ascold air flows into the valley where it is retained bythe surrounding hills.

Study site A was a 30 x 30 m plot on pasturewhich gently sloped towards the north-east. This sitewas unfenced to allow both sheep and cattle to graze,and was selected because it had a high density ofScotch thistles growing on it (0.23 nr2). Study site Bwas a 6 X 6 m plot of bare soil on which a number ofthistle seedlings had established naturally, and towhich a further 27 were transplanted (total numberof plants = 64).

METHODS

Flowering phenologyA total of 275 plants were growing at sites A and B.Every two weeks the numbers of flowering plants atthese two sites were noted. A plant was recorded asflowering from the time the first flower head openeduntil the last flower head died.

Effect of different pollination treatments onseed productionThree plants were chosen from a group of a dozenplants that were growing along a fence line adjacentto site B during early March of 1982. All of the plantswere flowering and numerous bees were present,ensuring that adequate cross-pollination would occur.Six terminal buds on each plant were chosen andtreated with a household insecticide spray to kill anysmall insects, such as thrips, which may have beenpresent and acted as pollinators. Four of these budson each plant were men enclosed in a wire frameover which white muslin was stretched and tiedsecurely at the base. When the buds flowered two ofthe enclosed flowers per plant were self-pollinatedby hand using a soft paint-brush. This was repeateddaily until the flower died. The other four buds perplant, two of which were covered in muslin, receivedno treatments. Thus, a total of six buds were cross-pollinated by the usual pollinators of this species, sixbuds were self ed, and six buds remained unpollinated.

The mature seed heads were removed and left todry for a week. The heads were then opened in themanner described below and the numberof shrunkenand normal seeds recorded. The normal seeds werethen germinated in an incubator at 20°C and 12hours of light. The remaining ungerminated seedswere dissected and the number of empty seedsrecorded.

Seed production and fertilitySeeds were collected by removing all unopened butmature seed heads (i.e., floral tissue had withered)from every thistle growing in a 2.5 ha paddockadjacent to site B (n = 26 plants). A random sampleof 30 seed heads was then drawn from this collection.Each head was cut transversely about lcm above thebase of the receptacle and the seeds removed. Theseed head was then dissected and any remainingseeds removed. Two seed forms were found,"normal" and "shrunken". The mean number ofseeds of all types was 211+21 seeds per flower head.

The shrunken seeds were discarded and thenormal seeds from the 30 seed heads were mixed.Eight samples of 50 seeds were then randomlyselected. These were put to germinate in an incubatorat 20°C and 12 h light. Any ungerminated seedsremaining 48 hours after the last germination weredissected. A number of hollow seeds were found andtheir numbers were recorded. The small number offilled seeds that didnot germinate were not recorded.Data concerning the production of these differentseed types were subsequenty obtained from a sampleof six seed heads collected from site A throughoutthe year.

Dispersal of seedsAn experiment was designed to investigate theefficiency of wind in dispersing C. vulgare seedsfrom a single plant. This plant was 1 m high andproduced 89 flower heads which yielded 18,800seeds based on an estimate of 211 seeds per seedhead. All thistles surrounding this plant were removedprior to the start of the experiment. A hinged circularseed trap, partitioned into a central area with fourequal areas surrounding it (area = 0.06 m2), wasfitted around the base of the plant. Sixteen seedtraps, 10 cm deep, were constructed from plastictubs. These tubs, of equal area to the partitions in thebasal seed trap, were arranged in four lines runningnorth, south, east, and west. They were placed atdistances (measured from the centre of the traps) of0.33 m, 0.67 m, 1.0 m, and 1.5 m from the stem of theplant. These traps, half filled with water, were buriedso that the top of the trap was level with the soilsurface. Thesetrapswere visiteddaily and the numberof seeds in each recorded before removal.

Longevity of seeds in the soilIt is known that many seeds, particularly those witha hard testa, can remain viable in the soil for manyyears (Harrington 1972). Popay et al. (1987) have


demonstrated this for seeds of nodding thistle(Carduus nutans). Casual observation of the effectsof soil disturbance, with the subsequentproliferationof thistle seedlings, suggested that C. vulgar e seedsremain viable when incorporated into the soil seedbank. An experiment was designed to try and quantifyaspects of this phenomenon.

Forty-five replicates of 100 seeds werewithdrawn at random from a bulk seed samplecollected previously. These replicates were placedin forty-five open plastic petri dishes to allow formicrobial and predator action. Fifteen of these disheswere buried at each of three depths. These depthswere 2 cm, 10 cm, and 20 cm, which correspondedapproximately to the top, middle, and bottom of thetopsoil. The petri dishes were not drilled to providedrainage. However, it is unlikely that the moisturecontent of the soil in the petri dishes was differentfrom the surrounding soil because capillary actionshould ensure even distribution of moisture. Freewater would collect in the bases of the petri dishesonly when the surrounding soil was itself saturated.

At intervals of three, six, and twelve monthsafter placement, five dishes from each depth wererecovered. Seeds were sieved from the soil and theviability of the seed estimated using trizoliumtetrachloride. This colourless, water solublecompound is reduced to a red form by living tissue(Colbry et al. 1961). Prior laboratory testing showedno significant differences in viability estimatesbetween germination trials and those obtainedthrough staining. These results are detailed inMichaux (1984) together with a discussion on thedifficulties associated with this technique.

Temperature requirements for germination

Nine replicates of three 9 cm diameter petri dishes(27 dishes in total), lined with Whatman filter paperand containing 100 seeds, were placed at differentpositions along a thermogradient plate. The lowesttemperature attained by the thermogradient platewas 7°C. The temperature across the centre of eachpetri dish was calculated from a temperature-distancegraph obtained from steady state readings ofthermometers placed along its length. Full details ofthe temperatures at which individual petri disheswere kept are given in Michaux (1984), but rangedfrom9oCto40°C. Seeds were arranged individuallyalong the equator of thepetri dish, with approximatelyequal numbers either side of this line. Seeds weredefined as having germinated when radicle lengthreached 1 mm, germinated seeds being counted and

removed every 24 hours. The filter paper was keptmoist with distilled water throughout theexperiment.

Two separate experiments were sequentiallyrun on the thermogradient plate, one using old seedthe other fresh, in order to see if there were anydifferences in germination characteristics. Old seedhad been collected 10 months prior to the start of theexperiment, sun dried on newsprint, and stored on alaboratory shelf in cork-stoppered glass vials. Freshseed had been collected from plants growing in thetwo study sites the day prior to the start of theexperiment (February, 1983). Data for old seedswere collected over 7 days (no germination on day1) and the experiment terminated when the fastestgerminating dishes had reached maximumgermination percentages, i.e., when no furthergermination occurred. Data for the new seedswere collected over 12 days (no germination onday 1, and no data collected on day 9). Thisexperiment was terminated after 12 days because theequipment was required for undergraduate teachingcourses.

Periodicity of seedling emergenceThe method described is similar to that used byRoberts & Chancellor (1979). Seeds were collectedduring the peak flowering period in December fromplants growing in the two study areas. Two woodenboxes, each measuring 50 X 25 X 12 cm, were filledto within 3 cm of the top with sterilised peaty loam.Two batches of 1000 seeds were drawn at randomfrom the bulk collection, and each mixed withsufficient soil to fill the boxes. The two boxes wereplaced in the open above ground level, and coveredwith mesh. One of the boxes was watered wheneverthe soil showed signs of drying out, the other receivedno additional watering other than rainfall. At the endof each month seedlings were counted and removed,and the soil was stirred to a depth of 3 cm to bringfresh seeds to the surface.

Vegetative growthFollowing germination, the young seedling rapidlygrows a number of main roots that allow the plant tobecome established quickly. This initialestablishment is followed by rosette growth beforevertical growth is initiated. Growth rates wereinvestigated by tagging all plants within randomlychosen quadrats at each study site (n = 20 plants atsite A, n = 21 plants at site B), and measuring thediameter or height (whichever was appropriate) attwo weekly intervals.

Michaux—Biology ofCirsium vulgare 405

RESULTS

Flowering phenologyThe results of flowering phenology are summarisedin Fig. 2. For this sample of 275 plants, floweringlasted from the middle of October to the middle ofMarch, a period of five months, with a peak in thesecond half of December. Although the peak periodof flowering of this sample is representative, therange of flowering time is probably affected by thesample size. All 275 plants flowered, the individualduration of flowering varying with the size of theplant Large plants with several hundred buds can beexpected to be in flower for six weeks. Subsequentto flowering all the plants died.

Effect of different pollination treatments onseed productionThe results from the effect of different pollinationtreatments on the production of different seed typesare given in Table 1. An ANOVA performed on theraw data showed a significant interaction termbetween pollination treatment and seed type (F ratio= 90.8, P>F = 0.000, d.f. = 4).

The data indicate that non-pollination results inshrunken seeds and self-pollination in hollow seeds.The hollow seeds present in the seed heads that werenon-pollinated resulted from self-pollination causedby the build up of pollen within the wire and muslincovers that surrounded the flower head. The highlevel of shrunken seeds in the self-pollinated seedheads is a reflection of the inefficiency of the self-pollinating technique. The levels of self- and non-pollination in the control are consistent with otherresults (see Table 2).

Seed production and fertilityThe data from this study are presented in Table 2.The important conclusion from these data is that

liA M J J A S O N D J F M

19S2/83

Fig. 2 Flowering phenology based on a sample of 275 C.vulgare plants at s ites A and B. Counts recorded fortnightlyfrom April 1982 through to March 1983.

Table 1 Effects of different pollination treatments onthe proportions of different seed-types of C. vulgareproduced. All numbers are mean percentages with 95%confidence intervals.

non- self- cross-pollination pollination pollination

shrunken 85±8 31±27 3±3hollow 13±6 63±28 5±3viable 1±4 6±8 92±6

Table 2 Seasonal variation in fertility of samples of C. vulgare seeds from January 1982 untilJanuary 1983. All figures are means with 95% confidence intervals. ND = no data.

Month

JanuaryMayJuneNovemberDecemberJanuary

No. of capitulaexamined

3066666

No. seedsper capitulum

211±21207140236±50345±1032821118340151

% shrunken

41222199619

613211314

% hollow

11157513

ND53171517313

% viable

86155130

411681169513


Fig. 3 Dispersal of seeds from asingle plant 1.0 m high, based ontrap counts at the distances fromthe stem indicated. Prevailing windfrom the south-west.

fertility (i.e., realised fecundity) varies with time.During the main flowering period (i.e., December -January) the majority of seeds produced by a singleplant are viable and fertility is at a maximum. Asmall number of shrunken and hollow seeds areproduced during this period because of low levels ofnon-pollination and self-pollination respectively.As the season progresses, two factors come into playwhich cause a decrease in fertility. The first of theseis a decrease in the density of flowering plants as theflowering season ends, resulting in an increase inself-pollination, and a corresponding increase in thenumber of hollow seeds produced.

The second factor is the decrease in number ofpollinators, mainly Apis mellifera and Bombus spp.,resulting in non-pollination and the production ofshrunken seeds. The results from this study suggestthat low densities of flowering plants resulted in adecrease in fertility prior to falling pollinatornumbers. At the beginning of the flowering seasonthere is a rapid increase in fertility as the density offlowering plants increases. Because pollinators arealready active prior to the start of the floweringseason, a low level of non-fertilisation was recordedduring November and December.

Dispersal of seedsThe results for the numbers of seeds trapped at givendistances from the plant are summarised in Fig. 3.This diagram shows that more seeds are dispersed inthe downwind direction (between north and east)beyond 0.33 m from the plant, i.e., beyond a third ofthe plant height.

The numbers per trap were then converted intodensity measures, which were used to calculate thenumber of seeds falling within the areas sampled bythose traps. The totals for each area were thensummed and this figure expressed as a percentage ofthe estimated number of seeds produced by theplant. These results are presented in Table 3. Of theestimated 18 800 seeds produced by theplant, 17 200(91 %) are calculated to have fallen in a circle with adiameter of 1.5 times the plant height.

Longevity of seeds in the soilThe results of this experiment are given in Table 4.Decrease in seed viability is clearly affected by bothlength and depth of burial, and, as demonstrated bythe two-way ANOVA, by an interaction effectbetween the two. The best fit exponential decay


curves for the results of burial at 20 cm and 10 cm aregiven in Fig. 4. Seeds buried just below the surfaceeither germinate or are destroyed through insect ormicrobial activity. Very few can be expected toremain viable (as estimated by TTC staining). Thoseburied at greater depths show an exponential decayin viability, with some indication that this rate ofdecay decreases with depth. Numbers of viable C.vulgare seeds in the soil seed bank are maintainedthrough a combination of annual importation offresh seed and induced dormancy in a proportion ofolder seed, that proportion being related to both ageand depth of burial.

Temperature requirements for germinationThe results are summarised in Fig. 5 and 6. In Fig. 5the mean germination percentage, rounded to thenearest whole number, was plotted againsttemperature. This was repeated for each day that theexperiment ran, resulting in six separate "curves"for old seeds (Fig. 5A) and ten for fresh seeds (Fig.5B). Following the analysis suggested by Thompson(1970) the graphs were then simplified to aid compari-son. This was achieved by calculating the maximumand minimum temperatures at which 50% of themaximum observed germination occurred, for eachday that this level was reached. This is done by read-ing these temperatures from the graphs in Fig. 5where the 50% germination line cuts the curves.

Table 3 Analysis of seed dispersal data. Plant height =lm. Estimated number of seeds = 18800 (89 capitula X211 seeds/capitulum). Estimated % of seeds fallingwithin 1.5 X plant radius = 91.5%.

Sector radius Area(m2)

Density( 2 )

No. of seedsin sector

0-0.18m.0.18-0.33m.0.33-0.67m.

0.67-1.00m.

1.00-1.50m.

0.060.281.07

1.73

3.93

Total seed

7202080272022202100291030801210150031103390113018603950

40580730590560780133052065013503330112018303880

17200

These temperatures are plotted against time inFig. 6. The best fit quadratics through these pointsare also given in Fig. 6. The two curves summarisegermination characteristics including the maximum,minimum, and optimum temperatures for germina-tion (Thompson 1970). The optimum temperaturefor germination is at the turning point of eachparabola, which for old seeds is 20°C and for freshseeds is 23.5°C. The maximum and minimum temper-atures of germination for both types of seeds haveextrapolated values of approximately 32°C and 7°C,respectively. The two types of seeds also differ inrate of germination and maximum observed germina-tion percentage. Fresh seeds have both slower rates,and lower percentage germination than old seeds.

Periodicity of seedling emergenceThe seedling counts are summarised in Fig. 7. Theresults show that most seeds germinate as soon assufficient moisture is present. The phenology ofseedling emergence is thus synchronised with rainfall.The majority of seeds are dispersed betweenNovember and March which, under normal rainfallpatterns in this area, produces two thistle crops - onederived from early germinating seeds, the otherfrom early autumn germination following increasedrainfall in March or April. Finally, the youngseedlings which were present during frosts, whenminimum air teperatures of -2°C. were recorded,appeared to be unharmed.

Vegetative growthThe results of vegetative growth are summarised inFig. 8. The plants at site A were already wellestablished when the study started in April (meandiameter 54± 11 cm), but continued to grow until the

Table 4 Results and analysis of burial and recovery datafor Cirsium vulgare seeds. Raw data is for number ofseeds stained with trizolium tetrachloride (maximumpossible = 100).

2cm.Retrieval Time

Depth of Burial10cm. 20cm.

3 months 1,0,0,0,06 months 3,1,1,0,012 months 2,1,0,0,0

30,14,13,7,616,15,10,9,620,8,7,6,3

44,33,28,22,2127,19,19,17,612,12,9,6,3

depthtimedepth*time

d.f.

224

Anova s.s. F-value P>F

2443.2 34.82 .0001564.4 8.04 .0013635.0 4.52 .0046


20 "

12 15 18 21 24

Length of burial (months)

eeds

in-o

ISm

?rof

Z

z

100 -

80 -

60 -

40 -

20 -

nU -

i

v\

i

B

>-^ T

6 9 12 15 18 21 24

Length of burial (months)

Fig. 4 Decrease in numbers of seeds stained withtrizolium tetrachloride as a function of time. A: Decaycurve for seeds buried to 20 cm depth. B: Decay curve forseeds buried to 10 cm depth. Error bars are 95% confidenceintervals. Best fit exponential curve generated and drawnby computer. A y = 62.3 X lO"0078" r2 = 0.94B y = 43.7 X lO"0071" ^=0.64.

middle of May. During early July the plot wassubjected to heavy density grazing by cattle whichresulted in considerable damage to the rosettes. Thisdamage stimulated regrowth with the result that bylate September the mean rosette diameter had returnedto predamage levels. From the middle of Augustvertical growth was initiated resulting in a periodwhen plants increased both in diameter and height,but by early October lateral growth had ceased andall growth was concentrated in height increase.

The results from site B are similar. Rosettegrowth continued for slightly longer than for thelarger rosettes at site A which, together with the

100

90 •

10 20 30 40

Temperature (°C)

100 i

Temperature! C)

Fig. 5 Germination characteristics of old (A) and freshseeds (B). Horizontal bar represents 50% of the maximumobserved germination in each case. Each line representsthe results for one day.

effects of damage in stimulating regrowth, suggeststhat lateral growth is inhibited by some internalfeedback mechanism rather than by environmentalcues such as temperature or photoperiod. Vertical


a Old seeds y=23.145-2.092x + 0.049X2 R2=0.94

• Fresh seeds y = 42.848- 3.254x +o.O7lx2 R2=o.74

1 4 -

12 -

1 0 -

8 -

S -

4 "

2 -

10 20 30 40

Temperature C

Fig. 6 Summarygraphofthegerminationcharacteristicsof old and fresh seeds. Best fit parabolas generated anddrawn by computer.

growth was synchronous in both areas which suggeststhat lengthening days may have cued this response.The mean maximum height of plants in the two areaswas not significantly different (P>0.2) despite themean maximum diameters being significantlydifferent (/»<0.0001).

DISCUSSION

The peak flowering period for the sample of plantsstudied was in the second half of December, with arange between October and March. However, it isusually possible to find some Cirsium vulgare plantsflowering at most times of the year. It is probable thatplants flowering in late autumn originate from seedsdispersed early in the main flowering period, or fromseeds that have been brought to the surface from theseed bank during the winter or early spring. It isnormal for thistles to live for eight to nine months inthe rosette stage. However, with the acceleratedgrowth expected during the spring and early summer,and again in the early autumn after rain, it is likelythat these plants could complete their developmentwithin a single season, behaving as annuals.

Local populations of this species appear to belargely self-infertile. This phenomenon was alsoreported by Sempala-Ntege (1969) for Englishpopulations that he sampled, but appears to be atvariance with results reported for Dutch populationsby van Leeuwen (1981). Van Leeuwen concludedthat "absence ofcross-pollination resulted in reduced

120-,

100-

80-

60-

40-

20-

0Jan Feb Mar Apr Mag Jun Jui Aug Sep r 20

£-10

Jan Feb Mar Apr May Jun Jul Aug Sep

600 i

500-

400-

300-

200 •

T3

$ 4 0 -

1 30-

20-

1 0 •

0 I I I •.• IJan Feb Mar Apr May Jun Jul Aug Sep

Month

Fig. 7 Upper Details of local rainfall pattern and numberof frosts for January through to October 1982. Lower:Seedling emergence pattern in two seed boxes keptoutsideover the same period. Solid shading watered, cross hatchedunwatered.

achene production....", but lack of quantitative dataconcerning the magnitude of this reduction makes acomparison of results difficult From his descriptionit would appear that a similar phenomenon operatesin Holland, but at much reduced level.


Fig. 8 Lateral (solid line) andvertical growth (broken line) basedon measurements taken from41 C.vulgare plants from April 1982through to January 1983 at sites AandB.

D J

1982/83

The bases of plant self-infertility have beendiscussed by Heslop-Harrison (1978), who notesthat a sporophytic self-incompatibility system isdeveloped principally in the Cruciferae and theCompositae. In this system incompatible pollengrains are inhibited from developing while still onthe stigma, either before or shortly after the pollentube has emerged. The genetic basis for this isbelieved to be a single sterility locus with a variablenumber of alleles existing at the locus. In thesporophytic system, pollen carries the parental(diploid) genotype and any shared sterility allelebetween pollen and stigma results in incompatibility.

If such a system operates in C. vulgare then thesituation must be more complex than outlined abovebecause, independent of the number of alleles at thesterility locus, self-pollination should always resultin an absence of viable seeds. Details of theincompatibility system of this species may explainthe differences already noted between the resultsreported by Sempala-Ntege (1969) and this paperwith those of van Leeuwen (1981).

Although C. vulgare requires cross-pollinationto set fertile seed - a somewhat surprising resultfrom this study considering the opportunist nature ofthe weed - this is achieved by the majority of plantsflowering over a restricted time period whenpollinators are active. Only those plants that flowerin the main flowering period, or where plants aregrowing in sufficient density, will contributesubstantially to the following generation.

Seeds of this species have an attached pappusallowing for wind dispersal. However, the results ofthis study suggest that this is an inefficient dispersalmechanism for the majority of seed. It is estimatedthat only 9% of the seed was dispersed beyond 1.5 m

from the plant used in this experiment. This estimateseemed low, particularly when viewed against theresults indicated in Fig. 3. Two reasons account forthis probable underestimation of the percentage ofdispersed seeds. Firstly, seeds with a pappus tendedto swirl around the ground surface, therefore theseed traps effectively sampled an area greater thanthe area of the trap. This could have been minimisedby laying out additional seed traps, or by not buryingthe seed traps. Secondly, because seeds could notescape once trapped, there was no further possibilityof subsequent, longer distance dispersal. It is difficultto see how one might overcome this problem.

As an additional check on the validity of thisestimated dispersal figure, data from the field trialswere collected. An estimate of the number of seedsthat had fallen in one of the original 3x 3 m quadratsof site A was calculated. A corner quadrat waschosen in which three plants had matured, producing194 000 seeds (918 flowersX 211 seeds). The numberof small seedlings growing in this quadrat wasestimated to be 4 800 which, from survivalprobabilities (Michaux 1984), were produced by113 000 seeds. Assuming no seeds had been lost tothe seed bank and thatnoimportationof seed occurred(or they were equal) it was calculated that 58% of theseeds produced had fallen within that quadrat.

A final piece of field evidence is presented inFig. 9 which summarises the analysis of thistledistribution in study area A. The observed resultswere obtained from the distribution of thistles in theoriginal 100 3 X 3 m quadrats that site A was dividedinto. The expected values were generated using thePoisson distribution and a %2 goodness of fit testperformed (Kershaw 1964). The observeddistribution is highly clumped. Such a distribution


30 -,

20-

<D

cr10-

0 1 2 3 4 5 6 >7

Number of plants per quadratFig. 9 Histogram showing observed (full) and expected(cross-hatched) distribution of numbers of thistle rosettesper 3 X 3 m. quadrat. Observed data based on the original100 3 X 3 m quadrats that site A was divided into. Expectednumbers generated using a Poisson distribution with mean(number of plants/quadrat) of 2.11. %2 = 48.4, P < 0.001,6 f)

can be explained in a number of ways, but the mostparsimonious explanation is that it is a reflection ofthe distribution of the preceding generation. Thisclumped distribution is consistent with limiteddispersal.

Sheldon & Burrows (1973) investigated therelative efficiency of Compositae "dispersal units"(pappus and seed) of a number of species in aidingwind dispersal under a given set of conditions. Theyconcluded that a number of factors affect dispersaldistance. Some of these relate to the structure of thedispersal unit, the most important of which is thecomplexity of the pappus unit. Those compositeswith complicated pappus structures such as pappushairs (like C. vulgare) have lower terminal velocitiesand higher aerodynamic drag coefficients, and henceremain airborne longer.

A number of external factors were also consideredto have important effects on dispersal efficiency.Sheldon & Burrows (1973) concluded that theoccurrence of a convective current has greater effectthan the strength of horizontal air movement which,in any case, may detach pappus from seed if it is toostrong. The effect of relative humidity on the openingand closing of the involucre bracts, on the force withwhich the seeds are held in the receptacle, and on theopening of the pappus is described in Dandeno(1905) and Small (1918). The height from which aseed disperses also affects its dispersal distance, as

do details of the surrounding terrain. The mainconclusion of their work is that primary projectorydistances are generally in the order of a few metres.It should be stressed that seeds have the potential forfurther dispersal, provided that they remain attachedto the pappus. However, it would seem that thepappus is not a very efficient means of dispersal,even under "ideal" conditions.

Experimental and field observations of otherstudies tend to confirm these conclusions. Poole &Cairns (1940) investigated the dispersal of ragwortseeds (Senecio jacobaea) from a large infestation.They calculated that 60% of the seeds were depositedwithin the infestation and that most of the restremained in the capitula. Approximately 0.5%became windborne with approximately 80% of thesebeing deposited within 37 m. They conclude thatonly a total of 0.1% of seeds would have beentransported further than 37 m, predominantly in thedownwind direction.

These results appear general; wind dispersal isnot an efficient means of seed dispersal in the sensethat the great majority of seeds fall in the immediatevicinity of the parent plant (Augspurger 1986;Augsperger & Franson 1987; Forcella & Woods1986; Sharpe & Fields 1982). In comparison withseed dispersal distances reported by Werner (1975)for seeds of Dipsacus sylvestris Huds., which haveno wind dispersal structures, it is apparent that forthe majority of seeds the dispersal distance is similarwhether wind dispersal structures are present or not.Differences are apparent, however, in extremedispersal distance which are a feature of winddispersed seeds. As Augspurger (1986) notes "therelative importance of mean and extreme dispersaldistances is unknown".

Long distance dispersal of only a small percentageof C. vulgare seeds, combined with its self-incompatibility and high mortality rates for veryyoung seedlings (Michaux 1984), suggests thatsuccessful long distance dispersal in this specieswould be a rare event and that spread of infestationsis marginal. That is, infestations will increase in sizeeach year, but that this spread will be moderate.What will happen is that the density of plants withinthe infestation will increase each year. Datareportedin Michaux (1984) sugests that this increase will bein the order of a factor of 9 per year on pasture andconsiderably higher on bare ground. Seeds arecertainly not spread uniformly over a wide area, ashas been assumed by authors such as Auld et al.(1979) when modelling control strategies for fecundannuals and biennials. The rapid spread of this


species throughout New Zealand following itsintroduction is therefore likely to have been aided byhumans. Seeds were possibly moved from district todistrict with stock and plant products such as grassand cereal seed or hay.

After seeds are dispersed from the mature plantthe majority lie on or just below the ground surface,with the remainder becoming incorporated into thesoil seed bank. The number of C. vulgare seedswithin the soil seed bank will decline until freshseeds are added to the seed bank the followingseason. However, based on the results of this study,a proportion of seeds from earlier years will remainviable for longer than a year, and thus one can expecta steady buildup of C. vulgare seeds in the soil seedbank. At any one time the seeds in the soil seed bankwill therefore be of mixed age classes. Theproportions of different age classes should be in theform of an exponential series. This ability of C.vulgare seed to remain dormant if buried to sufficientdepth is not, as discussed previously, an uncommonphenomenon. Its importance with respect to the con-trol of this and other weeds is in minimising pasturedamage during the wet winter months. Over-stockingduring the winter will result in pasture damage and,by bringing viable seed to the surface, increase thelevel of thistle infestation the following season.

Seeds on the surface are exposed to lightAlthough it has not been established by this study,light is probably responsible for the differencesnoted in the germination characteristics of old andfresh seed. That is, light alters conditions withinseeds to enhance germination rate, lower optimumgermination temperatures, and increase maximumgermination percentages.

It has been established that germination percent-ages of C. vulgare seeds are affected by differentlight treatments (Grime et al. 1981). These authorsused three light treatments, full light, shade (2.4% offull light intensity), and dark. The germinationpercentages recorded were 71%, 75%, and 19%,respectively. This last figure is significantly diferentfrom the full light figure (P< 0.01). Their resultsshow that germination of seeds of this species isinhibited by the absence of light. Williams (1966)reported that an increase in germination percentagewas obtained when fresh C. vulgare seeds weretreated with thiourea, a compound known to over-come the light requirement for germination in somespecies. It is quite probable that the differences ingermination results reportedby Roberts & Chancellor(1979) for Cirsium vulgare seeds in the UK, and theresults reported in this paper, are due to this

phenomenon. It is possible that winter temperaturesin the UK were too low for germination during theexperiment conducted by Roberts & Chancellor, butas these workers failed to stir the soil in the wetwinter months, and thus failed to bring fresh seed tothe surface, germination would not be expected.

Light can inhibit or stimulate germination throughthe alteration of an equilibrium that exists betweentwo different forms of phytochrome (PR and PFR)within seed (Borthwick et al. 1952). PFR is activeandpromotesgermination. Theequilibrium is shiftedtowards this form by the absorbtion of red light (1 =630-660nm), and away from this form to the inactivePR by absorption of far-red light (1 = 730nm).Futhermore, PFR can be destroyed in the dark byenzymic action, PFR killer, or chemical degradation(Black 1969; Furuya 1968; Briggs & Rice 1972;Kendrick & Frankland 1976).

It would appear that there is insufficient PFR infresh C. vulgare seeds, and that the differences ingermination characteristics of fresh seeds alreadydescribed are a result of the phytochrome equilibriumproducing excess PR. The inhibition of germinationof buried seeds can be understood in terms ofreversion of PFR to PR and/or the destruction ofPFR in the dark. It is probable that inhibition ofgermination would also occur when seeds lie underan unbroken grass cover, because the light reachingthe seeds wouldbe enriched with far-red wavelengths(Vezina & Boulter, 1966), causing conversion ofPFR to PR. If this last conclusion is correct, then themost important cause of thistle infestation isinadequate sward cover on pastures in the late summerand early autumn when the majority of seed dispersaloccurs. Manipulation of grazing regimes during thisperiod has the potential to be included in an integratedapproach to thistle control.

This study suggests that when adequate rain fallsmassive germination of ripened seeds occurs, aconclusion also reached by Forcella & Wood (1986)for this species in Australia. Because seeds tend togerminate where pasture cover is minimal or absent,the young seedlings have limited competition forspace from useful pasture species. As they grow thedevelopment of a rosette kills surrounding grasses.Onceplantshavebecomeestablisheditisnotpossibleto control them through grazing manipulation, asdamage to established rosettes is compensated forby stimulating regrowth and is, in any case, undesir-able because of the probability of initiating a freshinfestation from seeds in the soil seed bank. Removingplants manually should be done after vertical growthhas been completed and food reserves have been


maximally depleted but before seed has set. The tim-ing of this will vary from year to year but, on thebasis of the results of this study, can be expected inOctober and November.

C. vulgare is a weed that requires repeated efforton the part of the pastoral farmer if it is to be main-tained at low infestation levels. The data reportedhere, together with an analysis of its associatedfauna reported elsewhere (Michaux 1989), make itclear why this is so. Intrinsic factors of the weed'sbiology, in particular those related to its reproductivecapabilities and seed germination characteristics,interact with extrinsic factors to produce high popula-tion growth potentials. The most important of theseextrinsic factors are the presence of a non-damaging,largely incidental fauna, and the suitability of muchof our pastoral land as thistle habitat. There is littlethat can be done to alter intrinsic factors, these aresimply biological characteristics of the weed, butconsiderable scope exists for the manipulation of theextrinsic factors to ensure that potential populationgrowth is not realised. Introduction of biologicalcontrol agents and manipulation of pastoral habitatsshould alter the plant-environment dynamics suf-ficiently to disadvantage C. vulgare.

ACKNOWLEDGMENTS

This work was carried out in partial fullfillment for thedegree of MPhil. at the University of Auckland. My thanksto Professor E. C. Young and Dr J. Ogden for discussionand comments on the manuscript. K. Richards drew figures1, 2, 3, 5, and 8. T. Belsen constructed the seed trap. L.Michaux typed the manuscript. Alan Jordan allowed me touse his land (site A) and maintained his good humourthroughout. Comments by the editor and an anonymousreferee to earlier manuscripts are gratefullyacknowledged.

REFERENCES

Augspurger, C. K. 1986: Morphology and dispersalpotential of wind-dispersed diaspores ofNeotropical trees. American journal of botany 73:353-363.

Augspurger, C. K.; Franson, S. E. 1987: Wind dispersal ofartificial fruits varying in mass, area andmorphology. Ecology 68:27-42.

Auld,B. A.;MenzK.M.;Medd,R. W. 1979: Bioeconomicmodels of weeds in pastures. Agro-ecosystems 5:69-84.

Black, M. 1969: Light-controlled germination of seeds.SymposiumoftheSocietyofExperimentalBiology,no. 23:193-217.

Borthwick, H. A.; Hendricks, S. B.; Parker, M. W.; Toole,E. H.; Toole, V. K. 1952: A reversiblephotoreaction controlling seed germination.Proceedings of the National Academy of SciencesUSA 38: 662-666.

Briggs, W. R.; Rice, H. V. 1972: Phytochrome-chemicaland physical properties and mechanism of action.Annual review of plant physiology 23: 293-334.

Colbry, V. L.; Swoffard, T. F.; Moore, R. P. 1961: Testsfor germination in the laboratory. US.Departmentof Agriculture Agriculture Yearbook^ Pp.433-443.

Dandeno, J. B. 1905: The parachute effect of thistle down.Science 22: 568-572.

Forcella, F., Woods, H. 1986: Demography and control ofCirsiumvulgare (Savi) Ten. in relation to grazing.Weed research 26: 199-206.

Furuya, M. 1968: Biochemistry and physiology ofphytochrome. In: Reinhold, L., Liwschitz, Y. ed.Progress inphytochemistry. London, Interscience.Pp. 347-405.

Grime, J. P.; Mason, G.; Curtis, A. V.; Rodman, LBand,S. R.; MowforthM. A. G.; Neal, A. H.; Shaw, S.1981: A comparative study of germinationcharacteristics in a local flora. Journal of ecology69:1017-1069.

Harrington, J. F. 1972: Seed storage and longevity. In:Kozlowski, T. T. ed. Seed biology. New York,Academic Press. Pp. 145-245.

Heslop-Harrison, J. 1978: Cellular recognition systems inplants (Studies in Biology, no. 100). London,Edward Arnold.

Kendrick, R. E.; Frankland B. 1976: Phytochrome andplant growth (Studies inBiology, no. 68). London,Edward Arnold.

Kershaw, K. A. 1964: Quantitative and dynamic ecology.London, Edward Arnold.

Leeuwen van, B. H. 1981: The role of pollination in thepopulation biology of the monocarpic speciesCirsium palustre andCirsiumvulgare. Oecologia57:28-32.

Michaux, B. 1984: Biological control of Scotch thistle{Cirsium vulgare). Unpublished M.Phil. Thesis,University of Auckland.

1989: Associated fauna at one site of Cirsiumvulgare (Savi)Ten., (Composite: Cynaraea). NewZealand entomologist 12: 13-16.

Poole, A. L.; Cairns, D. 1940: Botanical aspects of ragwort(Senecio jacobaea) control. DSIR researchbulletin, no. 82.

Popay, A. I.;Thompson, A.;Bell,D. D. 1987: Germinationand emergence of nodding thistle (Carduus nutansL.). 8th Australian weeds Conference, September1987.

Roberts, H. A.; Chancellor, R. S. 1979: Periodicity ofseedling emergence and achene survival in somespecies of Carduus, Cirsium, and Onopordum.Journal of applied ecology 16: 641-647.


Sempala-Ntege, F. H. J. 1969: Some aspects of thephysiology and ecology oiCirsiumpalustre (L.)Scop, and Cirsium vulgare (Savi) Ten.Unpublished PhD thesis, University ofLancaster.

Sharpe, D. M., & Fields, D. E. 1982: Integrating th effectsof climate andseedfall velocities on seed dispersalby wind: a model and application. Ecologicalmodelling 77:297-310.

Sheldon, J. C ; Burrows, F. M. 1973: The dispersaleffectiveness of the achene-pappus units of selectedCompositae in steady winds with convection.Newphytologist 72: 665-675.

Small, J. 1918: The origin and development of theCompositae. New phytologist 17: 69-94.

Thompson, P. A. 1970: Characterization of thegerminationresponse to temperature of species and ecotypes.Nature 225: 827-831.

Turin, T. G.; Heywood, V. H.; Burges, N. A.; Moore, D.M.; Valentine D. H.; Walters, S. M.; Webb, D. A.ed. 1976: Flora Europaea, volume 4. Cambridge,Cambridge University Press.

Vezina, P. E.; Boulter, D. W. K. 1966: The spectralcomposition ofnearultravioletandvisibleradiationbeneath forest canopies. Canadian journal ofbotany 44: 1276-1284.

Werner, P. A. 1975: A seed trap for determining patternsof seed dispersal in terrestrial plants. Canadianjournal of botany 53: 810-S13.

Williams, D. 1966: Variation in the germination of severalCirsium species. Tropical ecology 7: 1-7.

michaux—biology of cirsium vulgare

Documents