effect of environmental factors on seed germination and seedling emergence of invasive ceratocarpus...

DOI: 10.1111/j.1365-3180.2011.00896.x

Effect of environmental factors on seed germinationand seedling emergence of invasive Ceratocarpusarenarius

E EBRAHIMI & S V ESLAMIFaculty of Agriculture, Birjand University, Birjand, Iran

Received 2 February 2011

Revised version accepted 4 October 2011

Subject Editor: Lars Andersson, SLU Uppsala, Sweden

Summary

Ceratocarpus arenarius is a problematic and noxious

weed of dryland farming in North Khorasan, Iran.

Experiments were conducted to investigate the mecha-

nism of seed dormancy, as well as the effect of

environmental factors on germination and emergence

of this species. Results showed that the pericarp is the

major obstacle to seed germination; seeds without an

intact pericarp had germination rates exceeding 90%.

Ceratocarpus arenarius had identical germination rates

in either light ⁄dark and continuous dark conditions,

indicating that this weed species is non-photoblastic.

Germination was >35% over a range of alternating

light ⁄dark temperatures (10 ⁄5, 20 ⁄ 10, 25 ⁄ 15, 30 ⁄ 20 and

35 ⁄ 25�C), with maximum germination (96%) at

25 ⁄ 15�C. Ceratocarpus arenarius seeds germinated at

rates >20% in high levels of salinity (800 mM) and

osmotic potential ()1 MPa), indicating that this species

is tolerant to saline conditions and drought stress during

germination and early seedling growth. Maximum

germination of C. arenarius seeds occurred at a pH

range of 7–9. Seedlings emerged from burial depths

ranging from 0 (without covering with filter paper) to

6 cm, and the maximum emergence (94%) was observed

in seeds placed on the soil surface covered with three

layers of filter paper. This suggests that minimum- and

no-till systems would increase seedling emergence of this

species through maintaining crop residues and seeds on

the soil surface. These attributes, coupled with tolerance

to salinity and drought stress during germination,

should be taken into account when managing C. arena-

rius.

Keywords: seed dormancy, salinity stress, drought

stress, burial depth, establishment.

EBRAHIMI E & ESLAMI SV (2012). Effect of environmental factors on seed germination and seedling emergence of

invasive Ceratocarpus arenarius. Weed Research 52, 50–59.

Introduction

Ceratocarpus arenarius L. is native to Eurasia and is

distributed from eastern and south-eastern Europe to

eastern Asia. It generally occurs in dry climates with

100–400 mm precipitation and is found in deserts, arid

slopes, sands, wastelands and along roadsides. Cerato-

carpus arenarius is widespread throughout western,

northern and central Iran (Mozaffarian, 2007).

Although generally considered a plant of sandy areas

rather than an agronomic weed of cropping systems,

C. arenarius has become a problematic and noxious

weed in dry-land wheat (Triticum aestivum L.), barley

(Hordeum vulgare L.), lentil (Lens culinarisMedicus) and

peas (Pisum sativum L.) in North Khorasan province of

Iran. Ceratocarpus arenarius is a greyish summer annual

herb 5–30 cm tall in the Chenopodiaceae family and has

amphicarpy (i.e. produces aerial seeds above ground and

Correspondence: S V Eslami, Faculty of Agriculture, Birjand University, Birjand, Iran. Tel: (+98) 5612254041 9; Fax: (+98) 5612254050; E-mail:

[email protected]

� 2011 The Authors

Weed Research � 2011 European Weed Research Society Weed Research 52, 50–59

subterranean seeds in soil) (Gao et al., 2008). It

produces large numbers of aerial seeds (c. 4000 per

plant) covered by a thick pericarp, which tightly adheres

to the seed coat after seed dispersal (Mozaffarian, 2007).

In autumn, when the end of the growing season occurs,

above-ground parts of the C. arenarius are easily

detached from the soil surface and are dispersed by

wind over a long distance. Farmers usually use 1-year

fallow in their rotation system, and, as an anemocor

species, C. arenarius infests this fallow lands. Plants

cannot be hand weeded, as the leaves and fruits are

covered by spines and farmers prefer to burn this

noxious weed. However, in semiarid climates like North

Khorasan, burning crop lands destroys the organic layer

of the soil, and this results in increased soil erosion.

Most invasive plants primarily rely on seed dispersal

and seedling recruitment for population establishment

and persistence. Rapid spread of many invasive plants is

frequently correlated with germination and dormancy

patterns. Dormancy may be associated with the seed

coverings (e.g. pericarp, testa and in some cases the

endosperm), or it can be a function of the embryo itself

(Gu et al., 2003). Environmental factors, such as tem-

perature, soil solution osmotic potential, solution pH,

light quality, management practices and seed location in

the soil seedbank, affect weed seed germination and

emergence (Norsworthy & Oliveira, 2006). To under-

stand why C. arenarius is so troublesome, it is important

to gain a better understanding of the mechanism of seed

dormancy and how seeds germinate in response to

different environmental factors, such as light, tempera-

ture, solution osmotic potential, solution pH and burial

depth. Better understanding of C. arenarius seed germi-

nation and dormancy would improve the management

of this weed by facilitating models that explore the

influence of factors such as tillage and burial on

germination and emergence.

Although C. arenarius is a problematic weed of

North Khorasan dryland farming systems, no informa-

tion is available about the effect of environmental

factors on its germination and emergence biology.

Therefore, the objectives of the studies reported here

were (i) to investigate seed dormancy mechanism as well

as identify methods to break dormancy and (ii) to

determine the influence of different environmental

factors on the seed germination and seedling emergence

of C. arenarius.

Materials and methods

Site and seed description

Mature aerial fruits of C. arenarius were collected in

November 2008, from several wheat fields at Quchan

city, in Northern Khorasan, Iran (latitude = 32º58¢N,

longitude = 11º35¢E and 1300 m altitude). Seeds were

collected from 500 plants and pooled to obtain seed

samples. Up to the time of the experiment (1 month

after maturity), the seeds were stored in paper bags at a

constant temperature (4 ± 1�C). The 1000-seed weight

of C. arenarius with and without pericarp was

5.6 ± 0.46 and 2.8 ± 0.46 g, respectively.

General protocol for germination tests

Four replications of 25 seeds of C. arenarius (with or

without pericarp) were placed in 9-cm Petri dishes lined

with two discs of Whatman No. 1 filter paper, moistened

with either 5 mL deionised water or treatment solution

when required. The Petri dishes were sealed with

Parafilm to minimise evaporation and either placed

directly in the germination chamber or wrapped in two

layers of aluminium foil to exclude light prior to placing

them in the germination chamber. Germination tests

were conducted for 14 days at a light ⁄dark temperature

range of 25 ⁄ 15�C (12 ⁄ 12 h). Seeds were considered to

have germinated when the radicle emerged. The number

of germinated seeds was counted daily. Germination

rate (S) was calculated according to the following

Maguire�s formula (1962):

S ¼ E1

N1þ E2

N2þ . . .

En

Nnð1Þ

where En is the number of germinated seeds observed in thenth daily counting and Nn is the number of days after theseeds were put to germinate in the nth counting.

Seed dormancy

In a preliminary test, freshly harvested seeds with intact

pericarp placed in Petri dishes did not germinate under

normal laboratory conditions (as described earlier in

the general protocol for germination tests). Therefore,

the effects of the following treatments on seed germi-

nation were evaluated: (i) immersion in water at room

temperature (25 ± 1�C) for 36 h; (ii) chemical scarifi-

cation with concentrated (95%) sulphuric acid for 2, 3

and 5 min, followed by thorough rinsing with running

water; (iii) mechanical scarification (abrasion of the

seeds between two sheets of sand paper for 3 min); (iv)

removing the pericarp by hand but leaving the seed

coat; (v) cold moist stratification in damp sand at 1

and )8�C for 15 days; (vi) puncturing the pericarp

using a needle and (vii) control. To puncture the seed

pericarp, seeds were first soaked in distilled water for

2 days at room temperature. It should also be pointed

out that care was taken to only remove the pericarp,

not the seed coat.

Ceratocarpus arenarius seed ecology 51



Temperature and light

Experiments were conducted to determine the effects of

various fluctuating temperatures (10 ⁄ 5, 20 ⁄10, 25 ⁄15,30 ⁄ 20 and 35 ⁄25�C) on germination of seeds (without

pericarp) under light ⁄dark and continuous dark

regimes. These temperature regimes were selected to

reflect the temperature variation during the spring to

summer period in North Khorasan.

Salinity

In this experiment, seeds (without pericarp) were exposed

to ten levels of increasing salinity using NaCl solutions of

0, 5, 10, 20, 40, 80, 160, 320, 640 and 800 mM. These

salinity levels were chosen based on known saline

conditions in North Khorasan soils (Ebrahimi et al.,

2010). Petri dishes were incubated as described in the

general protocol under light ⁄dark regime.

Recovery from salinity

After 14 days, seeds in treatment solutions were no

longer germinating, so all germinated seedlings were

removed and ungerminated seeds of the highest salinity

treatment (800 mM NaCl) were rinsed with distilled

water and placed back in their dishes with 5 mL of

distilled water for 14 more days. If seeds germinated

after being rinsed with distilled water, then seed germi-

nation was assumed to have been inhibited by an

osmotic effect, as opposed to a specific ion effect

(Ungar, 1991). An osmotic effect is caused by solutes

in the environment that lowers the osmotic potential to a

point where germination or growth is inhibited.

Enforced dormancy and growth inhibition because of

osmotic stress can be alleviated after seeds are removed

from a saline environment. A specific ion effect is

because of the chemical influence ⁄ toxicity of a given ion,

and not an osmotic stress caused by that ion.

Solution osmotic potential

Ceratocarpus arenarius seeds were germinated (without

pericarp) in a cycle of 12 h light ⁄ 12 h dark in aqueous

solutions of polyethylene glycol 6000 with osmotic

potentials of 0, )0.1, )0.2, )0.4, )0.6, )0.8 and

)1.0 MPa, prepared by dissolving appropriate amounts

of PEG 6000 in deionised water (Michel, 1983).

pH

The effect of pH on seed germination (without pericarp)

was studiedusingbuffer solutions of pH4–10according to

the method described by Chachalis and Reddy (2000). A

2 mM potassium hydrogen phthalate buffer solution was

adjusted to pH 4 with 1 NHCl. A 2 mM solution ofMES

[2-(N-morpholino) ethanesulfonic acid] was adjusted to

pH 5 and 6 with 1 N NaOH. A 2 mM solution of HEPES

[N-(2-hydroxymethyl) piperazine-N-(2-ethanesulfonic

acid)] was adjusted to pH 7 and 8 with 1 NNaOH. Buffer

solutions of pH 9 and 10 were prepared with 2 mM tricine

[N-Tris (hydroxymethyl) methylglycine] and adjusted

with 1 N NaOH. Petri dishes were incubated under a

25 ⁄ 15�C light ⁄dark temperature cycle as described for the

general germination protocol described earlier.

Emergence depth

The effect of different planting depths on seedling

emergence of C. arenarius was investigated in a growth

chamber. Seeds (without pericarp) were buried at eight

different depths (0 cm or soil surface, 0.5, 1, 2, 4, 6, 8 and

10 cm) in 15-cm-diameter plastic pots. An additional

treatment included seeds placed on the soil surface

covered with three sheets of filter paper to provide

constant water supply to the seeds. The filter paper was

briefly removed during daily emergence assessment.

Control pots in whichC. arenarius seeds were not planted

were included to ensure that there was no residual

seedbank of C. arenarius in the study soil. Moist soil

was placed over sown seeds to the appropriate depth and

gently compacted. For each burial depth, four pots

(replicates), with 50 seeds per pot, were set up. Soil used

for this experiment was a loam comprised of 43% sand,

32% silt and 25% clay with 0.44% total organic matter

and a pH of 7.4. Pots were placed in a growth chamber set

at a light ⁄dark temperature of 25 ⁄ 15�C. The photoperiodwas set at 12 h with fluorescent lamps used to produce a

light intensity of 140 lmol m)2 s)1. Pots were watered

after seed sowing until each pot reached field capacity and

excess water leached from the base. Watering was

repeated weekly (uniformly to all pots) or as the soil

dried. Seedlings were counted as they emerged from the

soil for 30 days after initial burial. At the termination of

the experiment, seeds buried at 10 cm depth were recov-

ered to determine the fate of ungerminated seeds. The soil

was filtered using a 0.1-mm mesh metal sieve to recover

intact seeds, as well as seedlings that were rotting as a

result of failure to emerge after germination. This

procedure made it possible to distinguish between seeds

that remained dormant and germinated seeds that failed

to emerge because of excessive depth of burial.

Statistical analyses

All experiments were carried out twice as a completely

randomised design with four replicates per treatment.

The data of the experiments were pooled for analysis, as

52 E Ebrahimi & S V Eslami



there was no time-by-treatment interaction. A functional

three-parameter logistic model (Chauhan et al., 2006a)

of the form:

Gð%Þ ¼ Gmax=½1þ ðX=X50ÞGrate� ð2Þ

was fitted to the germination values (%) obtained at

different concentrations of NaCl or osmotic potential

using SigmaPlot (version 11.0, SyStat Software, Inc.,

Point Richmond, CA, USA). In this equation, G

represents the total germination (%) at NaCl concentrationor osmotic potential x, Gmax is the maximum germination(%), x50 is the NaCl concentration or osmotic potential for50% inhibition of the maximum germination, and Grate

indicates the slope. The seedling emergence (%) valuesobtained at different burial depths were fitted to a sigmoidaldecay curve (Norsworthy & Oliveira, 2006) of the form:

Eð%Þ ¼ Emax=ðexpð�ðx� x50=ErateÞÞ ð3Þ

where E represents the seedling emergence (%) at burialdepth x, Emax is the maximum seedling emergence, x50represents the depth at which emergence is reduced by 50%,and Erate indicates the slope. Transformation of data did notimprove homogeneity; therefore, ANOVA and regressionanalysis were performed on non-transformed percentagegermination data (GenStat, version 9.2, VSN InternationalLtd., Hemel Hempstead, UK).

Results

Breaking of dormancy

Seeds with the intact pericarp were deeply dormant, as

demonstrated by 0% germination (Fig. 1). Removal of

the pericarp by hand broke dormancy in 97% of seeds.

Sulphuric acid scarification also broke dormancy and

induced seed germination, with the greatest effect (57%

germination) at a chemical scarification time of 3 min.

Mechanical scarification improved seed germination

only by 13%. The remaining treatments resulted in

low germination values (slightly higher than controls).

Temperature and light

Ceratocarpus arenarius seed germination was not influ-

enced by the light regime, with almost identical results in

either light ⁄dark or continuous dark conditions (Fig. 2

A). However, incubation temperature had a significant

effect on seed germination with maximum and minimum

germination at 25 ⁄ 15�C (96%) and 10 ⁄ 5�C (38%),

respectively. The 20 ⁄ 10 and 30 ⁄ 20�C alternating tem-

peratures regimes increased seed germination to >85%,

although the warmest temperature regime (35 ⁄ 25�C)reduced germination to 43%. Furthermore, different

temperature regimes affected the rate of seed germina-

tion (Fig. 2B). The effect of alternating temperatures on

Cont

rol

Peric

arp

rem

oval

by

hand

Sulfu

ric a

cid

(2 m

in)

Sulfu

ric a

cid

(3 m

in)

Sulfu

ric a

cid

(5 m

in)

Mec

hani

cal s

carif

icat

ion

Peric

arp

punc

turin

gCh

illin

g (1

°C)

Chill

ing

(–8°

C)

Imm

ersi

on in

wat

er

Ger

min

atio

n (%

)

0

20

40

60

80

100

Fig. 1 Effect of different treatments on dormancy breaking of

C. arenarius. Vertical bars represent SED.

Ger

min

atio

n (%

)

0

20

40

60

80

100

Alternating temperature (C)10/5 20/10 25/15 30/20 35/25

Ger

min

atio

n ra

te (S

eed/

day)

0

4

8

12

16

20

A

B

Fig. 2 Effect of temperature and light on seed germination

percentage (A) and germination rate (B) of C. arenarius. Vertical

bars represent SED.




seed germination rate was very similar to their impact on

germination percentage; the maximum and minimum

germination rates were observed at 25 ⁄ 15 and 10 ⁄ 5�C,respectively.

Salinity

Ceratocarpus arenarius germination was >90% in

NaCl concentrations up to 40 mM, with germination

exceeding 75% even at 160 mM NaCl (Fig. 3A) and

reaching 20% even at 800 mM NaCl. The three-

parameter logistic model provided a satisfactory fit

for the response of seed germination to NaCl concen-

tration (Fig. 3A). Salinity also influenced the germina-

tion rate of C. arenarius (Fig. 3B). Increasing salinity

level to 160 mM caused a 30% reduction in germina-

tion rate compared with the control, with >80%

reduction at 800 mM NaCl. Recovering the ungermi-

nated seeds from the salinity level of 800 mM and re-

incubating them with distilled water resulted in a

germination of 70%.

Solution osmotic potential

Decreased solution osmotic potentials reduced germi-

nation percentage, as well as germination rate of

C. arenarius seeds. Seed germination was >75% up to

the osmotic potential of )0.4 MPa (Fig. 4A), but

declined to 25% at the osmotic potential of )1 MPa.

The three-parameter logistic model provided a satis-

factory fit for the response of seed germination to

osmotic potential (Fig. 4A). The rate of germination

for the control was 18.3 seeds per day, but only

2.2 seeds per day at an osmotic potential of )1 MPa

(Fig. 4B).

pH

Ceratocarpus arenarius seeds had >45% germination

over a pH range of 4–10 (Fig. 5A). Maximum and

minimum germination percentage occurred at pH 8

(96%) and pH 4 (46%), respectively. Variation in

germination rate over the tested pH range was parallel

to the germination percentage, so that the fastest and

G (%) = 94.12/[1+(X/400.72)1.53]r2 = 0.98

Ger

min

atio

n (%

)

0

20

40

60

80

100

NaCl concentration (mM)0 200 400 600 800

Ger

min

atio

n ra

te (S

eed/

day)

0

4

8

12

16

20

24

A

B

Fig. 3 Effect of NaCl concentration on seed germination


bars represent SED.

G (%) = 93.35/[1+(X/0.67)2.28]r2 = 0.96

Ger

min

atio

n (%

)

0

20

40

60

80

100

Osmotic potential (–MPa)0.0 0.2 0.4 0.6 0.8 1.0

Ger

min

atio

n ra

te (S

eed/

day)

0

4

8

12

16

20

24

A

B

Fig. 4 Effect of osmotic potential on seed germination percentage

(A) and germination rate (B) of C. arenarius. Vertical bars

represent SED.




slowest germination occurred at pH 8 (13.7 seed per

day) and pH 4 (5.7 seed per day), respectively (Fig. 5B).

Emergence depth

Ceratocarpus arenarius seedlings emerged at all planting

depths up to 6 cm, but the maximum emergence (94%)

occurred for seeds placed on the soil surface under three

layers of filter paper. Seeds on the soil surface without

covering showed slightly lower emergence (80%) than

those buried at 0.5 cm (85%) (Fig. 6A). The sigmoidal

decline model provided the best fit to the data for

C. arenarius emergence in relation to seeding depth

(Fig. 6A). Emergence was observed 1 day after sowing

(14%) for seeds placed on the soil surface beneath the

filter paper (data not shown). Examination of non-

emerged seeds recovered from a burial depth of 10 cm

showed that most seeds (95%) at this depth germinated

but seedling cotyledons failed to reach the soil surface.

The maximum emergence rate was observed for the

seeds placed on the soil surface, and increasing burial

depth drastically reduced the emergence rate (Fig. 6B).

Discussion

The pericarp was found to be the major impediment to

seed germination in C. arenarius, because its complete

removal resulted in the greatest germination (97%)

(Fig. 1). In contrast, cold stratification, immersion in

water, pericarp puncturing and mechanical scarification

had low to moderate effectiveness (<15%). Acid scar-

ification improved seed germination, but it was not a

complete success; seeds scarified for 3 min showed a

moderate increase in germination (57%). According to

Bewley and Black (1982), pericarp-imposed dormancy

could be related to interference with water uptake or

gaseous exchange (i.e. oxygen entry or carbon dioxide

dissipation), presence of chemical inhibitors in the coat

or prevention of the escape of inhibitors from the

embryo, modification of light reaching the embryo or

exertion of a mechanical restraint. Pericarp-imposed

dormancy has been observed in a number of other weed

species such as Anthemis cotula L. (Gealy et al., 1985),

Oryza sativa L. (weedy rice) (Gu et al., 2003), Zygo-

phyllum xanthoxylum Maxim. (bean caper) (Hu et al.,

G (%) = –118.93 + 55.16X – 3.53X2, r2 = 0.99

Ger

min

atio

n (%

)

0

20

40

60

80

100

pH of buffered solution4 5 6 7 8 9 10

Ger

min

atio

n ra

te (S

eed/

day)

4

6

8

10

12

14

16

A

B

Fig. 5 Effect of buffered pH solution on seed germination


bars represent SED.

E (%) = 89.7/[1+e–(x–3.7)/–1.58], r2 = 0.98

Emer

genc

e (%

)

0

20

40

60

80

100

Burial depth (cm)0 2 4 6 8 10

Emer

genc

e ra

te (S

eed/

day)

0

2

4

6

8

A

B

Fig. 6 Effect of seed burial depth on seedling emergence percentage

(A) and germination rate (B) of C. arenarius. Vertical bars

represent SED.




2010) and Hedysarum scoparium Fisch. (sweet vetch)

(Hu et al., 2009). Results from this study provided

evidence that C. arenarius seeds possess physical dor-

mancy rather than physiological dormancy, as seeds do

not require stratification pre-treatment to germinate.

The precise role of the pericarp in conferring seed

dormancy, however, cannot be confirmed, given the

limited scope of the present study. Thick pericarp in

species such as C. arenarius could be beneficial for long-

term seed survival in the soil in harsh dry environments.

Germination in species with a thick pericarp is only

likely to occur after rainfall that is adequate to decom-

pose seed pericarp; such rainfall is also likely to be

adequate to sustain weed seedling growth (Hu et al.,

2009).

Ceratocarpus arenarius seed germination was insensi-

tive to light, indicating that this is a non-photoblastic

weed species capable of germination whether buried or

exposed, provided moisture and temperature are suit-

able (Fig. 2A). Exposure to light stimulates germination

in many weed species, but there are species in which light

has no effect or even inhibits germination. Baskin and

Baskin (1998) reported that among 54 grass species,

germination of 28 was promoted by light, 13 were

unaffected by light or dark conditions, and 13 were

inhibited by light. Promotion of germination by light

has been associated with small, rather than large, seeds

(Milberg et al., 2000). Moreover, it has been reported

that hard seeds do not typically require light for

germination (Chauhan et al., 2006b; Chauhan & John-

son, 2008). In dry-land wheat in North Khorasan,

C. arenarius seeds germinate during the spring concur-

rently with a dense cover of wheat seedlings. Evidence

from our study suggests that seedlings of this weed

species are able to establish even beneath the leaf canopy

shade of a wheat crop.

Ceratocarpus arenarius seeds germinated over a

broad range of alternating temperatures (10 ⁄ 5, 20 ⁄10,25 ⁄ 15, 30 ⁄20 and 35 ⁄ 25�C), with optimum germination

between 20 ⁄10 and 30 ⁄20�C, coinciding with the opti-

mum temperature for germination rate (Figs. 2A and

B). Temperature outside this optimum range (i.e. 10 ⁄ 5and 35 ⁄ 25�C) reduced germination percentage and

germination rate, indicating that germination of this

weed species decreases during the cold months of

autumn and warm months of summer. This is not

surprising, as C. arenarius seedlings are often observed

during early to late spring in this region. Temperature

ranges identified as favourable for germination in this

weed species are observed in North Khorasan in late

March to April (Ebrahimi et al., 2010). The ability of

C. arenarius to germinate over a wide range of temper-

atures is consistent with observations of its emergence in

the field of this region over the spring and summer

months. Later-emerging C. arenarius seedlings have the

potential to escape control measures, such as post-

emergence herbicides that are usually applied to wheat

in late February and mid-March in North Khorasan.

Exposure to high saline concentrations in our study

decreased both germination percentage and germination

rate. Similar results were obtained by Osborne et al.

(1993) in a study of six species adapted to a semi-arid

climate in Western Australia. Germination of 20% seeds

of C. arenarius at 800 mM NaCl indicates greater salt

tolerance in this species compared with many other weed

species reported previously. Germination of nearly 80%

observed in C. arenarius at 160 mM NaCl is 4- to 40-fold

greater than that reported in Brassica tournefortiiGouan

(African mustard), Sonchus oleraceus L. and Galium

tricornutum Dandy (Chauhan et al., 2006a; b; c). The

parameter x50 of the fitted logistic model representing

the NaCl concentration required for 50% inhibition of

the maximum germination was 400.7, an additional

indication of high salt tolerance of this species during

germination. This parameter was only 89.6 for S. ole-

raceus (Chauhan et al., 2006a). Zia and Khan (2004)

also reported that Limonium stocksii Boiss, a known

halophytic species, had about 10% germination at

400 mM NaCl concentration. These results show that

C. arenarius is able to germinate even in highly saline

soils common in North Khorasan (Ebrahimi et al.,

2010). Ceratocarpus arenarius seeds demonstrated good

recovery (70%) after the treatment solution of 800 mM

NaCl was rinsed from the seeds and replaced with

distilled water, indicating that enforced seed dormancy

was mainly because of an osmotic effect, as opposed to

toxicity owing to an ionic effect. Most weed seeds are

situated close to the soil surface, where salt concentra-

tion varies because of continuous evaporation of

groundwater (Ungar, 1991). Rainfall can quickly leach

salt from the surface and supply water to the seed.

Therefore, for successful establishment of plants in

saline environments, seeds must remain viable at high

salinity and germinate when salinity decreases (Khan &

Ungar, 1997). Halophyte seeds are known to maintain

viability for extended periods of time during exposure to

high salinity and then germinate when salinity is reduced

(Keiffer & Ungar, 1995; Khan & Ungar, 1998). Such

seeds show a range of responses from partial to complete

germination recovery when salinity stress is alleviated

(Khan, 2002). Our results indicate that C. arenarius

seeds can withstand high salinity stress while maintain-

ing a viable seedbank for recruitment of new individuals.

Ceratocarpus arenarius seed germination was affected

substantially by increasing water stress. The tolerance of

a particular weed species to water stress appears to be

related to its ecology, for example, Eslami (2011) found

that a xeric population of Chenopodium album L. from




Iran maintained >65% seed germination up to an

osmotic potential of )0.4 MPa, while decreasing osmo-

tic potential from 0 to )0.4 MPa caused an 80%

reduction in germination (9% germination) of a mesic

population of the same weed species from Denmark.

Results from our study show that C. arenarius is fairly

tolerant to water stress during germination and can

tolerate dry soils. Clifford et al. (2004) in their research

on Caperonia palustris L. that has been introduced as a

drought-tolerant species found that germination was

only 9% at an osmotic potential of )0.8 MPa, whereas

germination of C. arenarius seeds at )0.8 and )1 MPa

osmotic potential was 45 and 25%, respectively. Rainfall

in Quchan is typically low during March and April, but

is likely to be sufficient for C. arenarius germination

(Ebrahimi et al., 2010). The osmotic potential required

for 50% inhibition of maximum seed germination (x50)

of C. arenarius (determined from the fitted model) was

considerably greater ()0.67 MPa) than values reported

for other weed species (Chauhan et al., 2006a,b,c;

Eslami, 2011). Under conditions of extreme tempera-

tures, high soil salinity and water deficit, germination is

typically delayed or completely inhibited, depending on

the intensity and duration of stress, as well as the genetic

background of the seed. Under drought stress, reduced

water potential of the germination medium is reported

as the cause of slow seed germination (Bradford, 1995),

which is similar to osmotic stress experienced under salt

stress. Therefore, it could be argued that seeds that

germinate rapidly under salt stress could also withstand

low water potential and germinate rapidly under

drought stress, and vice versa. Similar physiological

mechanisms may facilitate rapid seed germination under

different conditions (Foolad et al., 2007). The drought

tolerance of C. arenarius seeds appears to be an adap-

tation to the limited and unpredictable rainfall of the

habitats that this species occupies (Ebrahimi et al.,

2010).

The ability of this species to germinate over a wide

pH range indicates that it can adapt to a wide range of

soil conditions and soil pH is not a limiting factor in

germination. This feature is common for invasive weed

species, and it potentially allows C. arenarius to invade

diverse habitats. However, germination of C. arenarius

was greatest at the pH range of 7–9. A pH of 10 as well

as more acidic pH values greatly reduced germination

rates. These results suggest that C. arenarius germinates

fastest in basic soil conditions, which are common

throughout the major crop production regions of North

Khorasan (Ebrahimi et al., 2010).

Ceratocarpus arenarius seedlings emerged from all

burial depths up to 6 cm, but no emergence was

observed from seeds buried at 8 and 10 cm. Lower

emergence from uncovered seeds on the soil surface

compared to those buried at 0.5 cm is not surprising, as

limited soil-to-seed contact and water availability are

known to limit germination on the soil surface (Ghor-

bani et al., 1999). Seeds placed on the soil surface and

covered with filter paper showed the greatest emergence

percentage. This suggests that germination of seeds on

the soil surface may be increased under field conditions

by the presence of cereal crop residue, which creates

greater soil–seed contact and preserves moisture. At

deeper soil depths, light and seed size are usually the

limiting factors for seedling emergence (Benvenuti et al.,

2004; Gardarin et al., 2010). Our results indicate that

light is not required for C. arenarius seed germination.

Larger seeds often have greater carbohydrate reserves

and are able to emerge from greater depths of burial

(Baskin & Baskin, 1998). According to the fitted model,

the seeding depth that decreased C. arenarius emergence

by 50% was 3.7 cm. Decreased emergence at increased

planting depth has been reported in several weed species,

including Conyza canadensis L. (Nandula et al., 2006),

Senna obtusifolia L. (Norsworthy & Oliveira, 2006) and

B. tournefortii (Chauhan et al., 2006c). The fact that

C. arenarius seeds are able to germinate at a depth of

6 cm indicates that it could escape control with pre-

emergence herbicides. Moreover, shallow burial with

tillage is unlikely to reduce its seedling emergence.

Emergence of recovered seeds buried at 10 cm showed

that failure to emerge was almost entirely the result of

fatal germination (95%), rather than depth-imposed

dormancy. This suggests that naked seeds of C. arena-

rius cannot establish a persistent seedbank. Seeds with

intact pericarp, however, might behave differently, as the

pericarp appears to prevent germination while it

encloses the seed. Such seeds are likely to persist in the

soil seedbank during adverse conditions, such as

drought, because of pericarp inhibition. Pericarp-

imposed dormancy is an ecological adaptation that

determines timing of germination to ensure optimal

seedling survival rates and favours seed persistence in

arid conditions (Hu et al., 2009).

Our data suggest that C. arenarius is well adapted to

the dry-land cropping systems where it is a problem,

including no-till systems. Moreover, herbicide-based

management of C. arenarius might be difficult because

of its emergence patterns. In fact, emergence after final

post-emergence herbicide applications or from greater

depths could contribute to a lack of season-long control

in many weed management programmes.

Removal of the pericarp may have biased the results

of this study by affecting the sensitivity of seed to light.

The great germination percentages observed in our

study would likely not occur in C. arenarius under field

conditions because of the physical dormancy imposed by

the pericarp; weathering and microbial decay of the




pericarp are necessary for ending dormancy. However,

using seeds with intact pericarps for these experiments

would have greatly reduced germination, making iden-

tification of environmental factors with the greatest

effect more difficult to identify. As pericarp removal is

required for maximum germination, soil disturbance in

conventional tillage systems could increase C. arenarius

emergence and deplete the seedbank. In contrast, use of

a no-till cropping system could reduce C. arenarius

germination, as this system may not damage the seed

pericarp.

Further research is required to elucidate details of

C. arenarius seed germination, especially those related to

the influence of the pericarp. However, the present study

provides preliminary information on the effect of the

pericarp on seed dormancy and on environmental

factors affecting seed germination. Longer-term studies

are needed to determine the impact of management and

climatic factors on the persistence of C. arenarius

seedbanks. This is important information required for

developing management strategies for this weed species.

Acknowledgements

We would like to acknowledge the University of Birjand

for financial support of this work. The authors wish to

thank Dr. Sarah Ward and Dr. Gurjeet Gill for their

comments on the manuscript and advice on language

revision.

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