Regeneration capacity from buds on roots and rhizomesin five herbaceous perennials as affected by timeof fragmentation

J. Liew • L. Andersson • U. Bostrom •

J. Forkman • I. Hakman • E. Magnuski

Received: 21 December 2012 / Accepted: 24 July 2013 / Published online: 2 August 2013

� Springer Science+Business Media Dordrecht 2013

Abstract Variation in seasonal sprouting pattern

from roots and rhizomes of perennial herbaceous

plants influence the success of plant proliferation

ability, invasiveness and escape from weed control

measures. The latter often rely on methods, which

repeatedly fragment the underground system, thereby

trigger adventitious and axillary buds to sprout, and

consequently reduce the amount of stored energy. If

carried out at times when no re-growth occurs,

treatments will have little effect on weed populations,

but cost much in terms of labour and energy. The

purpose of this experiment was to determine the

seasonal variation in bud sprouting capacity after

fragmentation. Five troublesome perennial weed spe-

cies, collected in northern and southern Sweden, were

grown outdoors in Uppsala, Sweden (N 59�490, E

17�390), from May 2009 to January 2010. Cut root and

rhizome fragments, taken at two weeks intervals from

July to January, were used to evaluate bud sprouting

capacity, which was statistically analyzed using

generalized additive models. In Elytrigia repens from

southern Sweden and Sonchus arvensis sprouting

capacity was significantly impaired during a period

from September to November. In Equisetum arvense

and Tussilago farfara sprouting was low between July

and November where after it increased. In contrast,

Cirsium arvense and E. repens from northern Sweden

sprouted readily throughout the period. Except for

E. repens, a model by populations was significantly

better than one based on latitudinal origin. The result

suggests a species-specific timing of treatments in

weed management, avoiding the non-effective autumn

period for E. arvense, S. arvensis and T. farfara, and in

some cases in E. repens.

Keywords Dormancy � Vegetative

reproduction �Weed biology � Disturbance

Introduction

The perennial species Cirsium arvense (L.) Scop.

(creeping thistle), Elytrigia repens (L.) Desv. ex

Nevski (common couch), Equisetum arvense L. (field

horsetail), Sonchus arvensis L. (perennial sow-thistle)

and Tussilago farfara L. (colt’s foot) are all pioneers in

open and ruderal habitats. They are also among the

most troublesome perennial weeds in Scandinavian

agriculture and all propagate from buds below ground.

In the rhizomatous species E. repens, E. arvense and

T. farfara, axillary buds develop at the nodes along the

length of the underground system. Furthermore,

J. Liew � L. Andersson � U. Bostrom (&) �J. Forkman � E. Magnuski

Department of Crop Production Ecology, Swedish

University of Agricultural Sciences, P.O. Box 7043,

750 07 Uppsala, Sweden

e-mail: ullalena.bostrom@slu.se

I. Hakman

School of Natural Sciences, Linnaeus University,

Barlastgatan 11, 391 82 Kalmar, Sweden

123

Plant Ecol (2013) 214:1199–1209

DOI 10.1007/s11258-013-0244-4

E. arvense also has the capacity to regenerate from

tubers. In C. arvense and S. arvensis, adventitious buds

are formed on vertical and horizontal roots and at the

base of the shoot.

Cirsium arvense is native to Europe and the east

northern hemisphere and has been classified as one of

the most invasive plants world-wide (Tiley 2010).

Sonchus arvensis is found in the temperate areas of the

northern and southern hemisphere (Lemna and Mes-

sersmith 1990). Both species can be found on disturbed

areas, waste land, along roadsides and riversides and

they are among the most problematic agricultural

weeds in Scandinavia, as well as in other temperate

areas (Lemna and Messersmith 1990; Salonen et al.

2008; Tiley 2010). As reviewed by Werner and Rioux

(1977), Elytrigia repens is a serious weed of cultivated

crops in most agricultural areas. Its distribution extends

throughout Europe, Australia, New Zealand and the

temperate zones of Asia and North and South America,

but it is characterised mainly as a ‘‘cool-season’’ grass.

Equisetum arvense, is native to the arctic and temper-

ate regions of the northern hemisphere. It was, together

with C. arvense and E. repens, mentioned among ‘‘the

world’s worst weeds’’ on arable land by Holm (1977).

Tussilago farfara is native to Europe and adjacent

Asia. It can be found growing wild by roadsides,

hedgerows, fields and waste ground and has been

reported as an agricultural weed in organic crops in

Northern Europe (Nkurunziza and Streibig 2011).

Non-chemical measures to control these species

when they occur as weeds on arable land rely on labour

and energy intensive methods, which fragment the

roots and rhizomes and have the intention to trigger the

buds to sprout. The aim is to empty the storage organs

of nutrients by repeating the treatment after resprout-

ing, thereby reducing their capacity of regrowth.

However, there are indications that the effect varies

with season and that the seasonal sprouting pattern

varies between the five plant species (Hakansson

1969; Hakansson and Wallgren 1972; Fykse 1974;

Williams 1979; Brandsæter et al. 2010; Andersson

et al. 2013). The conditions required for induction and

release of dormancy is not only species specific, but

also ecotype specific, as demonstrated by e.g. Ofir and

Kiegel (2006). Bud dormancy, which is the inability to

initiate normal growth under otherwise favourable

conditions, is an adaptation to escape sprouting prior

to seasonal cold temperatures and/or drought in areas

where winters are harsh or summers dry. In perennial

plant species, bud dormancy is commonly regulated

by environmental cues like temperature and light

(McIntyre 1970; Horvath et al. 2003, and references

herein). As highlighted by Klimesova and Klimes

(2007, and references herein) seasonal changes in the

vegetative regeneration capacity of the bud bank make

it particularly sensitive to timing of disturbance.

For four of the species (C. arvense, E. arvense,

S. arvensis and T. farfara), we have recently shown a

seasonal pattern in the ability to sprout from undis-

turbed root/rhizome systems when the aboveground

biomass is removed (Andersson et al. 2013; Bostrom

et al. 2013). For E. repens, there seems to be a reduced

capacity to allocate energy to shoot production in the

autumn (Bostrom et al. 2013), which may affect the

capacity of rhizome buds to sprout.

Here, we investigated what happens if the root and

rhizome systems of the five species are cut into pieces,

just as they are in a field situation after soil disturbance

(e.g. by soil cultivation) in the autumn. This study

focused on the second half of the growing season since

it seems reasonable that a shift in resprouting capacity

of these perennial plants would occur in the autumn

before the onset of winter. In earlier studies (e.g.

Brandsæter et al. 2010; Andersson et al. 2013),

sprouting readiness was evaluated from the number

of emerged shoots above soil level from planted

fragments or defoliated plants. However, to our

knowledge, there are no results published on studies

done at the bud level.

We used a common garden experiment to test

whether there is a genetic component to the sprouting

phenology in populations originating from different

latitudes. Our hypotheses were that, (i) there is a

seasonal variation in bud sprouting capacity after

fragmentation of belowground roots, rhizomes and

tubers, respectively, and that, (ii) the reduction in

sprouting readiness starts earlier in populations from

northern Sweden than in populations from the south

when they are exposed to the same temperature and

photoperiod conditions.

Materials and methods

Plant material

In total four populations of each of five species (C. arvense,

E. repens, E. arvense, S. arvensis and T. farfara),

1200 Plant Ecol (2013) 214:1199–1209

123

collected in May and June 2008 in southern and northern

Sweden, respectively, were used in this common garden

experiment. Details of collection sites are presented in

Table 1. Fragments were planted in boxes (50 L) in June

2008. They were grown outdoors in a netted yard until

early November 2008, and subsequently stored in 4 �C in

darkness over winter. In late May 2009 (20 May for

C. arvense, S. arvensis and T. farfara, 26 May for E. repens

and E. arvense), root and rhizome pieces, 10 cm in length

for C. arvense, 10 cm for E. repens, 7.5 cm for E. arvense,

5 cm for S. arvensis, and 15 cm for T. farfara, were cut and

planted in pots (5.5 L, top Ø 19.5 cm, height 25.5 cm;

Soparco, Conde-sur-Huisne, France) filled with 3 L soil

(Hasselfors Garden; 85 % peat, 15 % sand, 180 g N m-3;

Neova, Hudiksvall, Sweden), and topped with 1 L soil

after planting. The pots were buried in a sandy soil, with

low infestation of perennial weeds, outside Uppsala,

Sweden (N 59�490, E 17�390). The soil surface in the pots

was about 5 cm above the surface of the surrounding soil.

Species were placed separately in the research field, in

close proximity to each other. Within species, the pots

were completely randomized to test dates. Nutrients were

added three timesbetween plantingand first exhumation as

commercial fertiliser (Wallco 51-10-43 plus micronutri-

ents; Cederroth International AB, Sweden). To each pot, in

total 2.8 mL Wallco, corresponding to 5 g N m-2, was

applied. Plants were irrigated when needed. Soil temper-

ature was registered with two Tinytag loggers (Tiny Talk;

Gemini Data Loggers, UK), buried at 5 cm depth in pots

(Fig. 1).

Test of sprouting capacity

To study the seasonal pattern of sprouting capacity,

two pots per population and species were randomly

chosen and exhumed at 2 week intervals, from 29 July

2009 to 25 January 2010. Soil was removed, below-

ground plant parts were carefully washed and roots

and rhizomes subsequently cut into fragments. Since

bud density is higher on roots of S. arvensis than on

C. arvense, we used fragments of 1 cm length for the

former and 3 cm for the latter. For the three rhizoma-

tous species, fragments were cut at 1 cm distance from

the node (1 cm on each side of it), i.e. single node

cuttings. For E. arvense, sprouting tests were also done

on tubers. Our aim was to have 10 fragments and 10

tubers per plant in each of two Petri dishes per plant.

This aim was fulfilled in all species most of the time,

but in C. arvense, fewer bud bearing roots were

available at about 25 % of the test dates, and in

E. arvense, fewer tubers were available in 2/3 of the

cases. For E. repens and T. farfara, the number of buds

which can give rise to a shoot equals the number of

fragments present. In E. arvense, the number of buds

was assumed to be twice the number of fragments

(Sakamaki and Ino 2006). Mean number of buds and

tubers per population and Petri dish, with standard

deviations is shown in Table 1.

For the root species, all sprouted buds with shoots

[0.2 cm in length, measured from the top of the bud

(i.e. where the brown periderm of the root and white

base of the sprout met for the root species), were

removed at the start of the sprouting test. For

rhizomatous species, only nodes and tubers with no

sprouted buds were used. The fragments and tubers

were placed in Petri dishes (Ø 90 mm) on double filter

paper (Munktell 1003; Munktell Filter AB; Falun;

Sweden) and moistened with 5 ml de-ionised water.

The Petri dishes were stacked on top of each other,

enclosed in aluminium foil and placed in 17/9 �C,

16/8 h, for 2 weeks.

In conclusion, the experiment encompassed five

species 9 2 regions (North and South) 9 2 popula-

tions 9 14 testing dates 9 2 plants (experimental

unit) 9 2 Petri dishes with 10 root/rhizome fragments

or tubers with a variable number of buds per dish.

After 2 weeks, all present buds were counted.

Based on previous knowledge and experience, we

considered buds producing shoots [0.5 cm to be

sprouting, and buds producing shoots\0.5 cm as non-

sprouting or less ready to sprout. Tubers were

considered as sprouting if a shoot broke the brownish

surface of the tuber.

Statistical analysis

Since the number of root buds on fragments of the

same length is highly variable, we evaluated sprouting

capacity based on proportions instead of absolute

numbers. We analysed data using generalized additive

models (GAMs), which, to our knowledge, has not

previously been much used in weed research. With

these models (Hastie and Tibshirani 1990), the relation

between the explanatory variable and the dependent

variable is not restricted to any particular shape.

GAMs are semi-parametric in the sense that a prob-

ability distribution still has to be known. Smoothing

spline functions replace the ‘‘slope’’-term of the linear

Plant Ecol (2013) 214:1199–1209 1201

123

Table 1 Details of collection sites, date of collection, mean number of buds per dish, with standard deviation for the populations

used in the experiment

Species Population Collection site Date of

collection

Mean number

of buds

Standard

deviation

C. arvense S1 N 55�520, E 12�580 6 May 11.26 4.30

S3 N 56�20, E 14�50 14 April 10.54 3.83

N1 N 64�20, E 20�40 2 June 11.80 4.59

N3 N 64�420, E 20�400 4 June 9.26 4.56

E. repens S1 N 56�100, E 13�520 14 April 10.02* 0.44

S3 N55�470, E13�320 6 May 9.73 0.54

N1 N 63�570, E 20�10 2 June 9.88 1.58

N3 N 63�510, E 20�110 5 June 9.83 1.39

E. arvense S1 N 56�140, E 12�360 15 April 18.83 (5.25) 3.22 (4.34)

S2 N 56�60, E 14�60 16 April 19.59 (7.48) 2.11 (3.90)

N1 N 63�570, E 20�10 2 June 18.48 (4.00) 2.90 (4.16)

N2 N 64�20, E 20�30 2 June 18.13 (3.21) 4.71 (3.55)

S. arvensis S1 N 56�100, E 13�520 14 April 11.94 4.84

S3 N 55�520, E 12�580 6 May 12.67 5.08

N1 N 64�410, E 20�380 4 June 8.40 3.81

N3 N 63�90, E 17�450 17 June 11.21 3.76

T. farfara S2 N 56�140, E 12�360 15 April 9.17 2.00

S3 N 55�520, E 12�580 6 May 8.90 2.14

N2 N 63�450, E 20�130 3 June 9.35 1.49

N3 N 64�410, E 20�370 4 June 9.48 1.26

For E. arvense, the mean number of tubers per dish and their standard deviation is given in parenthesis. Population identities follow

the naming in Andersson et al. (2013) and Bostrom et al. (2013)

* By mistake, more than 10 fragments were used in some dishes, so the total number of buds exceeds 10

Fig. 1 Daily mean soil temperatures from July 2009 to February 2010

1202 Plant Ecol (2013) 214:1199–1209

123

regression type of models, meaning that the curve is

allowed to bend in other ways than determined by

e.g. polynomials. Thus, no estimates of parameter

variables and intercepts are provided, and the output

from the model is commonly used for graphical

exploration. Approximate statistical inference can

still be made. The statistical analyses were per-

formed in SAS 9.2 (SAS Institute Inc, Cary, NC)

using the GAM procedure. The output of a GAM

analysis consists of a parametric part, a spline part

and a total deviance. A significant parametric part of

a GAM means that there is a linear trend over time.

A significant spline part should be interpreted as

there is a significant curvature in the trend over time.

With the GAM procedure, the linear part is tested

with a t test, and the spline function with a v2 test.

Since the spline function builds on the linear part of

the model, the linear part was included in the model,

also when it was not significant.

The proportion of sprouted buds in relation to total

number of buds (all present buds including the non-

sprouting) was modeled with a binomial distribution

and a logit link. The proportion of sprouted tubers

was modeled in the same way as described for buds.

The smoothing parameters for the cubic spline

functions of the non-parametric part of the model

were based on four degrees of freedom (d.f.), which

seemed reasonable based on graphical evaluation of

the fitted model as compared to observed data. The

species were analyzed separately. The following

comparisons were made: (i) a model with a single

curve was compared with a model with origin-

specific curves (i.e. two curves), and (ii) a model

with origin-specific curves was compared with a

model with population-specific curves (i.e. four

curves). Degree of complexity in the fitted model

was determined from approximate statistical tests, in

which the difference in deviance between a more

complex model and a simpler one was compared.

Due to over-dispersion, adjusted F tests, which are

more conservative than v2 tests, were used for this

purpose. Differences were considered significant at

level 0.05. To achieve a consistent graphical output,

all populations were modeled with a spline function,

although in some cases, the spline function was not

significant (meaning that a generalized linear model

could have been used instead of a GAM). To save

space, only P values for non-significant linear or

spline parts of the analyses are reported.

Results

For all species except E. repens, the significantly best

model consisted of population-specific curves (Figs 2,

3, 4). For E. repens, the best model was based on the

latitudinal origin of the plants.

Cirsium arvense

Although two populations of C. arvense showed a

decreasing trend in proportion of sprouting buds in

autumn (just before 23 September), the overall impres-

sion suggested no seasonality for this species (Fig. 2).

However, there were significant differences between the

populations (F10, 196 = 4.53, P \ 0.001). For population

S1, neither the linear nor the spline part of the analysis

was significant (t50 = -0.75, P = 0.454 andv32 = 5.61,

P = 0.132, respectively), meaning there seems to be no

seasonal pattern in sprouting ability of this population.

Until 7 October, the two northern populations showed

the same pattern of sprouting, but then started to diverge.

For population N1, the linear part of the GAM was not

significant (t49 = -1.62, P = 0.112). The two southern

populations behaved similarly from 3 November and

onwards, but differently in the beginning.

Sonchus arvensis

The predicted proportions of sprouting buds [0.5 cm

for S. arvensis show a clear reduction in sprouting

capacity during a period in the autumn (Fig. 2).

Sprouting was lowest between 8 September and 7

October. In the beginning of November, plants sprouted

almost as readily as in end of July. The difference

between populations was stronger than the regional

effect (F10, 198 = 3.02, P = 0.001). The populations

could easily be separated based on root morphology,

such as colour and texture, branching pattern and

number of root buds. For example, one of the northern

populations (N1) developed fewer buds (8.4 cm-1) than

the other three populations (11.2–12.7 cm-1) (Table 1),

and one of the southern populations (S3) had much

rougher root surfaces than the northern populations.

Equisetum arvense

There were considerable differences in the proportion

of sprouting buds [0.5 cm among populations for

Plant Ecol (2013) 214:1199–1209 1203

123

E. arvense (F10, 176 = 5.99, P \ 0.001), and the

reduction in sprouting readiness varied between them

(Fig. 3). From a minimum in August and September,

sprouting capacity increased steadily after 7 October

until December, when sprouting began to decrease in

two of the populations, one from each region.

For tubers, there was no clear pattern in sprouting

readiness (Fig. 3). One of the southern populations

(S1) sprouted most vigorously from tubers in October

to November, during the same period as when the

proportion of sprouting from buds was highest (the

linear part of the GAM was non-significant for tubers

of this population: t30 = 0.22, P = 0.827). In the

other southern population (S2), the proportion of

sprouted tubers increased from August to mid-Sep-

tember, decreased slightly until November, and then

started to increase. In the two northern populations,

sprouting from tubers decreased until November. In

population N1, a temporary increase in November–

December was seen, until finally decreasing again.

For population N1, the linear part of the model was not

significant (t26 = -0.62, P = 0.538); and for popu-

lation N2, the spline function was not significant

(v32 = 4.7, P = 0.195).

Elytrigia repens

For E. repens, a model with origin-specific curves

fitted the observations better than a model with a single

curve (F5, 214 = 8.95, P \ 0.001) (Fig. 4). In contrary

to the other species, a model with population-specific

curves did not fit the observations better than a model

with origin-specific curves (F10, 204 = 1.68, P =

0.088). Populations from the northern part of Sweden

had a higher sprouting capacity than populations from

the south during most part of the autumn. A decrease

in the proportion of sprouting buds in September–

October was detected for the southern region. Such a

decrease was not seen for populations from the

northern region. However, both spline terms were

C. arvense, south

Pop S1 Pop S2

C. arvense, north

Pop N1 Pop N2

S. arvensis, south

Pop S1 Pop S2

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

S. arvensis, north

20 Jul 8 Sep 28 Oct 17 Dec 5 Feb 20 Jul 8 Sep 28 Oct 17 Dec 5 Feb

20 Jul 8 Sep 28 Oct 17 Dec 5 Feb 20 Jul 8 Sep 28 Oct 17 Dec 5 Feb

Pop N1 Pop N2

Test date

Pro

port

ion

of s

prou

ted

buds

Fig. 2 Predicted

proportions of sprouting

buds[0.5 cm for C. arvense

and S. arvensis, two

populations of each species

from northern (N1, N3) and

southern (S1, S3) Sweden

from end of July 2009 to end

of January 2010. The fitted

GAM used 4 d.f. for

estimation of each

smoothing parameter.

For C. arvense population

N1, the linear part of the

GAM was not significant

and for population S1,

neither the linear nor the

spline parts of the GAM

were significant. The daily

mean soil temperature was

below 0 �C from the middle

of December and onwards

1204 Plant Ecol (2013) 214:1199–1209

123

significant: v32 = 71.2, P \ 0.001 and v3

2 = 28.6,

P \ 0.001 for the northern and southern region,

respectively.

Tussilago farfara

As in E. arvense, sprouting capacity in fragments of

T. farfara was most impaired in August and Septem-

ber, and increased after 7 October (Fig. 4). Sprouting

was low even in the beginning of the test period, and

was not resumed until almost a month later than for

E. arvense and S. arvensis. There was a rapid increase

in sprouting capacity during November for T. farfara.

Differences between populations were significant

(F10, 198 = 4.22, P \ 0.001). On 1 December, more

than 50 % of the buds sprouted in three of the

populations, while the fourth (S3) did not reach this

point until 11 January.

Discussion

In accordance with our first hypothesis, there was a

low or declining sprouting capacity in autumn in three

of the five species (E. arvense, S. arvensis and

T. farfara). Other studies on root fragments of S.

arvensis have also demonstrated reduced sprouting

during a period in the autumn (Hakansson 1969;

Hakansson and Wallgren 1972; Fykse 1974; Brandsæ-

ter et al. 2010). This has also been shown in T. farfara

(Fykse 1977; Bostrom et al. 2013). The reduction in

sprouting capacity during September–October found

in defoliated plants of E. arvense and T. farfara

(Bostrom et al. 2013) was not manifested after

fragmentation. Instead we registered constantly low

sprouting between end of July until end of October the

same year. Also Kvist and Hakansson (1985) noted

slow development of rhizomes and shoots for T.

farfara during August and September and Fykse

E. arvense, south

20 Jul 28 Oct 17 Dec 5 Feb

Pop S1 Pop S2

E. arvense, north

20 Jul 28 Oct 17 Dec 5 Feb

Pop N1 Pop N2

E. arvense tubers, south

20 Jul 28 Oct 17 Dec 5 Feb

Pop S1 Pop S2

0.0

0.4

0.0

0.2

0.2

0.4

0.6

0.6

0.8

1.0

0.8

1.0

0.0

0.4

0.8

0.2

0.6

1.0

0.0

0.2

0.4

0.6

0.8

1.0

E. arvense tubers, north

20 Jul

8 Sep 8 Sep

8 Sep 8 Sep 28 Oct 17 Dec 5 Feb

Pop N1 Pop N2

Test date

Pro

port

ion

of s

prou

ted

tube

rs /

buds

Fig. 3 Predicted

proportions of sprouting

buds[0.5 cm for E. arvense

and for tubers, two

populations from northern

(N1, N2) and southern (S1,

S2) Sweden from end of July

2009 to end of January 2010.

The fitted GAM used 4 d.f.

for estimation of each

smoothing parameter. For

tubers the linear part of the

GAM was non-significant

for S1 and N1; the spline part

was non-significant for N2.

The daily mean soil

temperature was below 0 �C

from the middle of

December and onwards

Plant Ecol (2013) 214:1199–1209 1205

123

(1977) suggested a tendency to dormancy during

autumn for this species. Data on E. arvense is sparse,

but in a Canadian study no decrease in shoot produc-

tion was found during the period between July and

September (Cloutier and Watson 1985).

The reduced biomass ratio between shoot and

rhizomes of E. repens in the autumn, reported by

Bostrom et al. (2013), seems to be expressed in

fragmented material in populations from southern

Sweden as a reduced proportion of sprouted buds. This

is contradictory to earlier studies where no restricted

sprouting in autumn was found (Brandsæter et al.

2010). However, it should be noted that in the southern

populations in our study at least 50 % of the buds

sprouted even in the period of low re-growth in this

species. In C. arvense, there was no reduction in

sprouting capacity, as was also suggested in studies by

Fykse (1977) and Brandsæter et al. (2010). The

reduced emergence from undisturbed root systems of

C. arvense grown under identical conditions

(Andersson et al. 2013) does not seem to be preserved

in fragmented roots. This indicates that mechanisms

other than innate dormancy cause the autumnal

incapacity to sprout from intact root systems of this

species.

Regarding differences between populations, there

were significant effects in the response to time of tests

for all species except E. repens. For a few populations

(C. arvense S1 and N1 (Fig. 2)), differences over dates

were small and may have been biologically insignif-

icant, but for the majority of populations, the propor-

tion of sprouting buds differed twofold or more over

sampling dates. These differences could, however, not

be attributed to the latitudinal origin of the plants, as

proposed for e.g. the summer dormant grass geophyte

Poa bulbosa (Ofir and Kiegel 2006). Our assumption

about earlier reduction in sprouting readiness for

northern populations (the second hypothesis) could,

thus, not be verified. Interestingly, the behavior of

E. repens was instead the opposite. In line with earlier

E. repens, south

Pop S1 Pop S2

E. repens, north

Pop N1 Pop N2

T. farfara, south

Pop S1 Pop S2

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

T. farfara, north

20 Jul 8 Sep 28 Oct 17 Dec 5 Feb 20 Jul 8 Sep 28 Oct 17 Dec 5 Feb

20 Jul 8 Sep 28 Oct 17 Dec 5 Feb 20 Jul 8 Sep 28 Oct 17 Dec 5 Feb

Pop N1 Pop N2

Test date

Pro

port

ion

of s

prou

ted

buds

Fig. 4 Predicted

proportions of sprouting

buds[0.5 cm for E. repens

and for T. farfara, two

populations of each species

from northern (N1, N2) and

southern (S1, S2) Sweden

from end of July 2009 to end

of January 2010. The fitted

GAM used 4 d.f. for

estimation of each

smoothing parameter. The

daily mean soil temperature

was below 0 �C from the

middle of December and

onwards

1206 Plant Ecol (2013) 214:1199–1209

123

studies (Hakansson and Wallgren 1976; Brandsæter

et al. 2010), plants from the northern region showed no

significant reduction in sprouting capacity in autumn.

However, for the southern region, a clear decline in the

proportion of buds producing shoots [0.5 cm was

detected. The decrease started August, and plants did

not recover until December. In a recent experiment

(Bostrom et al. 2013) we found a reduced shoot/

rhizome biomass ratio in autumn, but to our knowl-

edge, reduced sprouting from isolated buds is not

reported elsewhere. Further investigations are needed

to explain differences among regions.

To reduce the influence of environmental differ-

ences between collection sites, all populations were

grown outside Uppsala during 2008 before the exper-

imental start 2009. In four of the studied species, we

found no genetic differences between populations

from different latitudinal origins regarding timing of

sprouting in 2009. It is possible that any latitudinal

differences in sprouting phenology that would have

been expressed in their natural habitats were con-

cealed, since the rearing site of the mother plants was

Uppsala and not the original sites of the populations.

However, no differences between 2008 and 2009 in

timing of sprouting capacity, that could be attributed

to the rearing site of the mother plants, were found in

these populations (Andersson et al. 2013; Bostrom

et al. 2013). Maternal effects due to, e.g., nutrients and

disturbance history have been described in other

perennial species (Latzel and Klimesova 2010; Latzel

et al. 2010).

None of the species with reduced sprouting capac-

ity in the autumn ceased growth completely. At least

about 10 percent of the buds still produced shoots

[0.5 cm during the period of least sprouting. Thus,

the impaired sprouting capacity appears to be not

absolute, as often found in seed collects with varying

germination percentage at different levels of seed

dormancy. Alternatively, growth might have occurred,

but at a reduced speed during a certain period. This

partial or quantitative bud dormancy is induced at a

time of the year when temperatures are still adequate

for growth, but shortly followed by a period of

unfavourable conditions. The signals regulating bud

dormancy are species specific, but photoperiod and

cold temperature seem to be main factors in temperate

climate (Chao et al. 2007). In an earlier study, we have

shown that the impaired sprouting capacity in root

fragments of S. arvensis is probably induced by short

photoperiods (Liew et al. 2012). As reviewed by e.g.

Olsen (2010) bud dormancy in many woody perenni-

als is induced by decreasing photoperiod in autumn,

and later released by temperatures approaching a

growth inhibiting level. In one of few studies on bud

dormancy induction and release in herbaceous species,

Heide (2001) concluded that both processes were

regulated by photoperiod in Sedum telephium, i.e. no

chilling was required for the release. In contrast, endo-

dormancy in Euphorbia esula is induced by a combi-

nation of short photoperiod and cold temperature, and

released by a prolonged period of cold temperature

(Anderson et al. 2005). In our experiment, sprouting

approached a minimum when daily mean soil tem-

peratures were rarely below 5 �C for longer times, and

sprouting increased as soil temperatures went below

0 �C. The reduced sprouting, at a time well ahead of

growth inhibiting field temperatures, is of ecological

significance, and was clearly shown in E. arvense, S.

arvensis and T. farfara, and in southern populations of

E. repens. By avoiding emergence of shoots which are

likely to be killed by low temperatures, valuable stored

nutrients and growing points, i.e. the meristems, are

saved.

The reduction in sprouting capacity in the late

summer and early autumn for T. farfara may be a

consequence of the life cycle of this species, described

by Ogden (1974). Irrespective if originating from a

seed or from a rhizome bud, plants grow vegetatively

during summer. In the beginning of the autumn, plants

enter a sexually reproductive phase, and clusters of

flower buds are formed on the stem base and rhizomes

in addition to new leaves. Flowering occurs in the

early spring, whereafter the stock dies, and the

rhizomes fragmentise. In earlier experiments, we

observed that flower buds formed almost simulta-

neously in all plants from the same population. In

February–March, the plants started to flower, even

under dark and cold (?4 �C) storage. Together with

our recent results of other studies (Bostrom et al.

2013), showing the same pattern of flower bud

formation and burst, this suggests a photoperiodic

control of flower bud set, while release of flower bud

dormancy seems to be controlled by temperature and/

or time. It is possible that the production of new leaves

in this species is interrupted when flower buds start to

develop, and assimilates are allocated to a larger

extent to the rhizomes. Our results here, with isolated

nodes, suggest that this interruption is not completely

Plant Ecol (2013) 214:1199–1209 1207

123

explained by apical dominance, but due to dormancy

regulated within the bud. In a perennial grass, Ott and

Hartnett (2011) revealed that flowering tillers transi-

tioned a larger proportion of their buds to tiller, than

did vegetative tillers. They ascribed this difference to

controls of apical dominance, sustained bud out-

growth, and individual bud characteristics (i.e., exog-

enous and endogenous dormancy).

The sprouting capacity from tubers of E. arvense

seems to be population specific, with no clear seasonal

pattern (Fig. 3). Only in one of the populations (N1), a

vague decrease followed by an increase in sprouting

readiness in October could be discerned. Thus, it

seems likely that the reduced capacity of sprouting

from plants with intact underground systems (Bostrom

et al. 2013) and in fragmented rhizomes are not

preserved in the tubers. Few data is available on the

timing of tuber sprouting but Williams (1979) reports

that tubers, which had been detached from the

rhizome, sprouted readily in November.

In peas, the outgrowth of axillary buds is inhibited by

the terminal bud (e.g. reviewed by Shimizu-Sato and

Mori 2001), and the lower buds differ in their response

to broken apical dominance depending on position

(Shimizu-Sato and Mori 2001; Waldie et al. 2010). In

E. repens, several workers have shown a polarity in bud

dormancy (reviewed by Taylor 1995), with buds close

to the apex being less dormant than more basal ones

(McIntyre 1970; review by Taylor 1995). This may

explain the absence of absolute dormancy in T. farfara

and E. arvense, two other rhizomatous species, in our

study. We used only non-apical rhizome buds in the test

of sprouting capacity, and it is therefore possible that

apical buds would have behaved differently.

For S. arvensis, where root buds develop along the

whole length of the root system when the root diameter

exceeds 1–1.5 mm (Hakansson 1969), it is possible that

some buds are always capable of growth, but at a

reduced speed. To our experience, buds of this species

sprout fast and readily after formation, and it is rare to

find buds where the leaf primordia have not broken the

brownish periderm covering the root. However, the

length of the sprouts can vary considerably.

The ever-sprouting capacity in C. arvense and in E.

repens (although a lower proportion of buds sprouted

in the southern populations of E. repens during a period

in the autumn) would explain the success of these

species in disturbed habitats. Always being able to send

new photosynthetic organs up into the light, they catch

every chance to colonize new areas when the environ-

mental conditions permit. Alternatively, they produce

shoots in autumn which remain protected from frost

below soil surface until emergence in spring. Thanks to

a deep root system (C. arvense; Nadeau and Vanden

Born 1988) or high freezing tolerance (E. repens;

Schimming and Messersmith 1988), these species are

well adapted to survive the cold, dry winter conditions,

even in absence of a bud dormancy.

Besides having both high tolerance to frost (as would

be expected since the roots are located in the topmost

20 cm of soil; Schimming and Messersmith 1988), and a

reduced capacity of sprouting in the autumn, S. arvensis

also produce a great number of adventitious buds along

the root systems (in our experiment, up to four buds per

cm of roots have been found) which might add to

survival. Only a minor part of the buds will ever be able

to produce flowering shoots. In short, the species have

evolved successful reproductive strategies with maxi-

mum protection for new shoots to survive through

dormancy and high freezing tolerance, in combination

with maximum entities of reproductive organs.

To conclude, sprouting capacity in root buds of S.

arvensis and rhizomateous buds of E. repens from

southern Sweden, E. arvense and T. farfara are

impaired during a period in the autumn, and start to

increase in November if the underground system is

fragmented. This implies that land managers dealing

with these species, should not plan for repeated soil

cultivation during this period. Fragments of C. arvense

and E. repens from northern Sweden, and tubers of E.

arvense sprout readily throughout the period from late

July to late January, if the environmental conditions

permit. Where these species are the main problem they

may be efficiently controlled by repeated soil cultiva-

tion throughout the autumn.

Acknowledgments This study was funded by the Swedish

Research Council for Environment, Agricultural Sciences and

Spatial Planning and the Swedish University of Agricultural

Sciences.

References

Anderson JV, Gesch RW, Jia Y, Chao WS, Horvath DP (2005)

Seasonal shift in dormancy status, carbohydrate metabo-

lism, and related gene expression in crown buds of leafy

spurge. Plant Cell Environ 28:1567–1578

Andersson L, Bostrom U, Forkman J, Hakman I, Liew J,

Magnuski E (2013) Sprouting capacity from intact root

1208 Plant Ecol (2013) 214:1199–1209

123

systems of Cirsium arvense and Sonchus arvensis decrea-

ses in autumn. Weed Res 53:183–191

Bostrom U, Andersson L, Forkman J, Hakman I, Liew J,

Magnuski E (2013) Seasonal variation in sprouting

capacity from intact rhizome systems of three perennial

weeds. doi:10.1111/wre.12035

Brandsæter LO, Fogelfors H, Fykse H et al (2010) Seasonal

restrictions of bud growth on roots of Cirsium arvense and

Sonchus arvensis and rhizomes of Elymus repens. Weed

Res 50:102–109

Chao WS, Fooley ME, Horvath DP, Anderson JV (2007) Signals

regulating dormancy in vegetative buds. Int J Plant Dev

Biol 1:49–56

Cloutier D, Watson AK (1985) Growth and reproduction of field

horsetail (Equisetum arvense). Weed Sci 33:358–365

Fykse H (1974) Studium av Akerdylle. Utbreiing i Noreg,

Vokster og Kvile–dels jamforg med narstaande arter.

Forskning og Forsok i Landbruket 25:389–412 (in Nor-

wegian with German summary)

Fykse H (1977) Untersuchungen uber Sonchus arvensis L.,

Cirsium arvense (L.) Scop. und Tussilago farfara L. Ent-

wicklung sowie Translokation von radioaktiv markierten

Kohlenhydraten und MCPA. Sci Rep Agr Univ Norway 56

Hakansson S (1969) Experiments with Sonchus arvensis L. I.

development and growth, and the response of burial and

defoliation in different developmental stages. Ann Agr

Coll Sweden 35:989–1030

Hakansson S, Wallgren B (1972) Experiments with Sonchus

arvensis L. II. reproduction, plant development and response

to mechanical disturbance. Swedish J Agr Res 2:3–14

Hakansson S, Wallgren B (1976) Agropyron repens (L.) Beauv,

Holcus mollis L. and Agrostis gigantea Roth. as weeds–

some properties. Swedish J Agr Res 6:109–120

Hastie T, Tibshirani R (1990) Generalized Additive Models.

Chapman & Hall, London

Heide OM (2001) Photoperiodic control of dormancy in Sedum

telephium and some other herbaceous perennial plants.

Physiol Plant 113:332–337

Holm LG, Plucknett DL, Pancho JV, Herbeger JP (1977)

World’s worst weeds distribution and biology. University

of Hawaii, Honolulu

Horvath DP, Anderson JV, Chao WS, Foley ME (2003)

Knowing when to grow: signals regulating bud dormancy.

Trends Plant Sci 11:534–540

Klimesova J, Klimes L (2007) Bud banks and their role in

vegetative regeneration—a literature review and proposal

for simple classification and assessment. Persp Plant Ecol

Evol Syst 8:115–129

Kvist M, Hakansson S (1985) Rhythm and dormancy periods in

the vegetative development and growth of some perennial

weeds. Swedish University of Agricultural Sciences.

Department of Crop Production. Uppsala, Sweden. Report

156

Latzel V, Klimesova J (2010) Year-to-year changes in expres-

sion of maternal effects in perennial plants. Bas Appl Ecol

11:702–708

Latzel V, Klimesova J, Hajek T, Gomez S, Smilauer P (2010)

Maternal effects alter progeny’s response to disturbance

and nutrients in two plantago species. Oikos

119:1700–1710

Lemna WK, Messersmith CG (1990) The biology of Canadian

weeds. 94. Sonchus arvensis L. Can J Plant Sci 70:509–532

Liew J, Andersson L, Bostrom U, Forkman J, Hakman I,

Magnuski E (2012) Influence of photoperiod and temper-

ature on sprouting capacity in Cirsium arvense and Son-

chus arvensis root buds. Weed Res 52:449–457

McIntyre GI (1970) Studies on bud development in the rhizome

of Agropyron repens. 1. the influence of temperature, light

intensity, and bud position on the pattern of development.

Can J Bot 48:1903–1909

Nadeau LB, Vanden Born WH (1988) The root system of

Canada thistle. Can J Plant Sci 69:1199–1206

Nkurunziza L, Streibig JC (2011) Carbohydrate dynamics in

roots and rhizomes of Cirsium arvense and Tussilago far-

fara. Weed Res 51:461–468

Ofir M, Kiegel J (2006) Opposite effects of daylength and

temperature on flowering and summer dormancy of Poa

bulbosa. Ann Bot 97:659–666

Ogden J (1974) Reproductive strategy of higher plants. 2. repro-

ductive strategy of Tussilago farfara L. J Ecol 62:291–324

Olsen JE (2010) Light and temperature sensing and signalling in

induction of bud dormancy in woody plants. Plant Mol Biol

73:37–47

Ott JP, Hartnett DC (2011) Bud production and dynamics of

flowering and vegetative tillers in Andropogon gerardii

(Poaceae): the role of developmental constraints. Am J Bot

98:1293–1298

Sakamaki Y, Ino Y (2006) Tubers and rhizome fragments as

propagules: competence for vegetative reproduction in

Equisetum arvense. J Plant Res 119:677–683

Salonen J, Andersson L, Andreasen C, Semb Tørresen K (2008)

Key perennial weeds in arable crops in the Nordic coun-

tries. Proc. EWRS–NJF Workshop 387. Wageningen,

pp.3–4

Schimming WK, Messersmith CG (1988) Freezing resistance of

overwintering buds of four perennial weeds. Weed Sci

36:568–573

Shimizu-Sato S, Mori H (2001) Control of outgrowth and dor-

mancy in axillary buds. Plant Physiol 127:1405–1413

Taylor JS (1995) Apical dominance in rhizomes of quackgrass,

Elytrigia repens: the effect of auxin, cytokinins, and

abscisic acid. Can J Bot 73:307–314

Tiley GED (2010) Biological flora of the British Isles: Cirisum

arvense (L.) Scop. J Ecol 98:938–983

Waldie T, Hayward A, Beveridge CA (2010) Axillary bud

outgrowth in herbaceous shoots: how do strigolactones fit

into the picture? Plant Mol Biol 73:27–36

Werner PA, Rioux R (1977) The biology of Canadian weeds. 24.

Agropyron repens (L.) Beauv. Can J Plant Sci 57:905–919

Williams ED (1979) Studies on the depth distribution and on the

germination and growth of Equisetum arvense L. (field

horsetail) from tubers. Weed Res 19:25–32

Plant Ecol (2013) 214:1199–1209 1209

123