DOI: 10.1111/j.1365-3180.2011.00896.

Effect of environmental factors on seed germination and seedling emergence of invasive Ceratocarpus arenarius
E EBRAHIMI & S V ESLAMI
Faculty 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 mechanism of seed dormancy, as well as the eect 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 25C), with maximum germination (96%) at 25 15C. 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 79. Seedlings emerged from burial depths ranging from 0 (without covering with lter paper) to 6 cm, and the maximum emergence (94%) was observed in seeds placed on the soil surface covered with three layers of lter 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. arenarius. 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, 5059.

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 100400 mm precipitation and is found in deserts, arid slopes, sands, wastelands and along roadsides. Ceratocarpus arenarius is widespread throughout western, northern and central Iran (Mozaarian, 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 culinaris Medicus) and peas (Pisum sativum L.) in North Khorasan province of Iran. Ceratocarpus arenarius is a greyish summer annual herb 530 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: s_v_eslami@yahoo.com 2011 The Authors Weed Research 2011 European Weed Research Society Weed Research 52, 5059

Ceratocarpus arenarius seed ecology 51

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 (Mozaarian, 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 temperature, soil solution osmotic potential, solution pH, light quality, management practices and seed location in the soil seedbank, aect weed seed germination and emergence (Norsworthy & Oliveira, 2006). To understand 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 dierent environmental factors, such as light, temperature, solution osmotic potential, solution pH and burial depth. Better understanding of C. arenarius seed germination and dormancy would improve the management of this weed by facilitating models that explore the inuence 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 information is available about the eect 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 inuence of dierent environmental factors on the seed germination and seedling emergence of C. arenarius.

city, in Northern Khorasan, Iran (latitude = 3258N, longitude = 1135E 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 1C). 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 lter paper, moistened with either 5 mL deionised water or treatment solution when required. The Petri dishes were sealed with Paralm 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 15C (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 Maguires formula (1962): S E1 E2 En ... N1 N2 Nn 1

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

Seed dormancy

Materials and methods

Site and seed description

Mature aerial fruits of C. arenarius were collected in November 2008, from several wheat elds at Quchan

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 eects of the following treatments on seed germination were evaluated: (i) immersion in water at room temperature (25 1C) for 36 h; (ii) chemical scarication with concentrated (95%) sulphuric acid for 2, 3 and 5 min, followed by thorough rinsing with running water; (iii) mechanical scarication (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 stratication in damp sand at 1 and )8C for 15 days; (vi) puncturing the pericarp using a needle and (vii) control. To puncture the seed pericarp, seeds were rst 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.

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Temperature and light

Experiments were conducted to determine the eects of various uctuating temperatures (10 5, 20 10, 25 15, 30 20 and 35 25C) on germination of seeds (without pericarp) under light dark and continuous dark regimes. These temperature regimes were selected to reect the temperature variation during the spring to summer period in North Khorasan.
Salinity

2 mM potassium hydrogen phthalate buffer solution was adjusted to pH 4 with 1 N HCl. A 2 mM solution of MES [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 N NaOH. Buer 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 15C light dark temperature cycle as described for the general germination protocol described earlier.
Emergence depth

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 germination was assumed to have been inhibited by an osmotic effect, as opposed to a specic 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 specic ion effect is because of the chemical inuence 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 eect of dierent planting depths on seedling emergence of C. arenarius was investigated in a growth chamber. Seeds (without pericarp) were buried at eight dierent 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 lter paper to provide constant water supply to the seeds. The lter paper was briey removed during daily emergence assessment. Control pots in which C. 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 15C. The photoperiod was set at 12 h with uorescent lamps used to produce a light intensity of 140 lmol m)2 s)1. Pots were watered after seed sowing until each pot reached eld 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 recovered to determine the fate of ungerminated seeds. The soil was ltered 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

The eect of pH on seed germination (without pericarp) was studied using buer solutions of pH 410 according to the method described by Chachalis and Reddy (2000). A

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

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there was no time-by-treatment interaction. A functional three-parameter logistic model (Chauhan et al., 2006a) of the form: G% Gmax =1 X =X50 Grate 2

was tted 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 concentration or osmotic potential x, Gmax is the maximum germination (%), x50 is the NaCl concentration or osmotic potential for 50% inhibition of the maximum germination, and Grate indicates the slope. The seedling emergence (%) values obtained at different burial depths were tted to a sigmoidal decay curve (Norsworthy & Oliveira, 2006) of the form: E% Emax =expx x50 =Erate 3

the pericarp by hand broke dormancy in 97% of seeds. Sulphuric acid scarication also broke dormancy and induced seed germination, with the greatest eect (57% germination) at a chemical scarication time of 3 min. Mechanical scarication improved seed germination only by 13%. The remaining treatments resulted in low germination values (slightly higher than controls).
Temperature and light

where E represents the seedling emergence (%) at burial depth x, Emax is the maximum seedling emergence, x50 represents the depth at which emergence is reduced by 50%, and Erate indicates the slope. Transformation of data did not improve homogeneity; therefore, ANOVA and regression analysis were performed on non-transformed percentage germination data (GenStat, version 9.2, VSN International Ltd., Hemel Hempstead, UK).

Ceratocarpus arenarius seed germination was not inuenced by the light regime, with almost identical results in either light dark or continuous dark conditions (Fig. 2 A). However, incubation temperature had a signicant eect on seed germination with maximum and minimum germination at 25 15C (96%) and 10 5C (38%), respectively. The 20 10 and 30 20C alternating temperatures regimes increased seed germination to >85%, although the warmest temperature regime (35 25C) reduced germination to 43%. Furthermore, dierent temperature regimes aected the rate of seed germination (Fig. 2B). The eect of alternating temperatures on

A
100

80

Results
Breaking of dormancy

Germination (%)

60

Seeds with the intact pericarp were deeply dormant, as demonstrated by 0% germination (Fig. 1). Removal of
100

40

20

80

Germination (%)

B
Germination rate (Seed/day)
60

20

16

40

12

20

0
n) pu nc tur ing illi ng (1 Ch C) illi ng Im (8 me C rsi ) on in wa ter ntr ol in) in) tio n d an by h (2 m (3 m mi rif ica Co (5

al

id

id

id ac

rem ov

ac

ac

ca

ls

arp

Ch

ric

ric

ric

ica

0 10/5 20/10 25/15 30/20 35/25

Su lfu

lfu

lfu

arp

an

Su

Su

Pe

ric

ric

Pe

Me

Alternating temperature (C)

ch

Fig. 1 Effect of different treatments on dormancy breaking of C. arenarius. Vertical bars represent SED.

Fig. 2 Effect of temperature and light on seed germination percentage (A) and germination rate (B) of C. arenarius. Vertical bars represent SED.

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A
100 80 60 40 20 0 G (%) = r 2 = 0.98 94.12/[1+(X/400.72)1.53]

100 80 60 40 20 0
B

Germination (%)

Germination (%)

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

24 20 16 12 8 4 0

24 20 16 12 8 4 0

Germination rate (Seed/day)

200

400

600

800

Germination rate (Seed/day)

NaCl concentration (mM)

Fig. 3 Effect of NaCl concentration on seed germination percentage (A) and germination rate (B) of C. arenarius. Vertical bars represent SED.

0.0

0.2

0.4

0.6

0.8

1.0

Osmotic potential (MPa)

Fig. 4 Effect of osmotic potential 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 5C, respectively.
Salinity

Solution osmotic potential

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 threeparameter logistic model provided a satisfactory t for the response of seed germination to NaCl concentration (Fig. 3A). Salinity also inuenced the germination rate of C. arenarius (Fig. 3B). Increasing salinity level to 160 mM caused a 30% reduction in germination rate compared with the control, with >80% reduction at 800 mM NaCl. Recovering the ungerminated seeds from the salinity level of 800 mM and reincubating them with distilled water resulted in a germination of 70%.

Decreased solution osmotic potentials reduced germination 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 satisfactory t 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 410 (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

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100 80 60 40 20 0
B

100 E (%) = 89.7/[1+e(x3.7)/1.58], r2 = 0.98 80 60 40 20 0

Germination (%)

G (%) = 118.93 + 55.16X 3.53X2, r 2 = 0.99

Emergence (%)
B

16 14 12 10 8 6 4

8 6 4 2 0

Germination rate (Seed/day)

10

Emergence rate (Seed/day)

10

pH of buffered solution
Fig. 5 Effect of buffered pH solution on seed germination percentage (A) and germination rate (B) of C. arenarius. Vertical bars represent SED.

Burial depth (cm)

Fig. 6 Effect of seed burial depth on seedling emergence 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

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 stratication, immersion in water, pericarp puncturing and mechanical scarication had low to moderate eectiveness (<15%). Acid scarication improved seed germination, but it was not a complete success; seeds scaried 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, modication 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), Zygophyllum xanthoxylum Maxim. (bean caper) (Hu et al.,

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 lter 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 t 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 lter paper (data not shown). Examination of nonemerged 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).

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2010) and Hedysarum scoparium Fisch. (sweet vetch) (Hu et al., 2009). Results from this study provided evidence that C. arenarius seeds possess physical dormancy rather than physiological dormancy, as seeds do not require stratication pre-treatment to germinate. The precise role of the pericarp in conferring seed dormancy, however, cannot be conrmed, given the limited scope of the present study. Thick pericarp in species such as C. arenarius could be benecial for longterm 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 decompose seed pericarp; such rainfall is also likely to be adequate to sustain weed seedling growth (Hu et al., 2009). Ceratocarpus arenarius seed germination was insensitive to light, indicating that this is a non-photoblastic weed species capable of germination whether buried or exposed, provided moisture and temperature are suitable (Fig. 2A). Exposure to light stimulates germination in many weed species, but there are species in which light has no eect or even inhibits germination. Baskin and Baskin (1998) reported that among 54 grass species, germination of 28 was promoted by light, 13 were unaected 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 & Johnson, 2008). In dry-land wheat in North Khorasan, C. arenarius seeds germinate during the spring concurrently 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 25C), with optimum germination between 20 10 and 30 20C, coinciding with the optimum temperature for germination rate (Figs. 2A and B). Temperature outside this optimum range (i.e. 10 5 and 35 25C) 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 identied 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 temperatures is consistent with observations of its emergence in the eld of this region over the spring and summer

months. Later-emerging C. arenarius seedlings have the potential to escape control measures, such as postemergence 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 tournefortii Gouan (African mustard), Sonchus oleraceus L. and Galium tricornutum Dandy (Chauhan et al., 2006a; b; c). The parameter x50 of the tted 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. oleraceus (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 concentration 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 maintaining a viable seedbank for recruitment of new individuals. Ceratocarpus arenarius seed germination was aected 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

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Iran maintained >65% seed germination up to an osmotic potential of )0.4 MPa, while decreasing osmotic 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. Cliord 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 sucient 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 tted 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 temperatures, high soil salinity and water decit, 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 dierent conditions (Foolad et al., 2007). The drought tolerance of C. arenarius seeds appears to be an adaptation 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 79. 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 (Ghorbani et al., 1999). Seeds placed on the soil surface and covered with lter paper showed the greatest emergence percentage. This suggests that germination of seeds on the soil surface may be increased under eld conditions by the presence of cereal crop residue, which creates greater soilseed 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 tted 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 preemergence 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. arenarius cannot establish a persistent seedbank. Seeds with intact pericarp, however, might behave dierently, 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. Pericarpimposed 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 dicult because of its emergence patterns. In fact, emergence after nal 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 aecting the sensitivity of seed to light. The great germination percentages observed in our study would likely not occur in C. arenarius under eld conditions because of the physical dormancy imposed by the pericarp; weathering and microbial decay of the

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pericarp are necessary for ending dormancy. However, using seeds with intact pericarps for these experiments would have greatly reduced germination, making identication of environmental factors with the greatest eect more dicult 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 inuence of the pericarp. However, the present study provides preliminary information on the eect of the pericarp on seed dormancy and on environmental factors aecting 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 nancial 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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