Seasonal cycles in germination and seedling emergence of summer ...

Weed Science, 54:114–120. 2006

Seasonal cycles in germination and seedling emergence of summer and winter populations of catchweed bedstraw (Galium aparine) and wild mustard (Brassica kaber) Husrev Mennan

Ondokuz Mayis University, Agriculture Faculty, Department of Plant Protection, 55139 Samsun, Turkey

Mathieu Ngouajio

Corresponding author. Michigan State University, Department of Horticulture, Plant and Soil Science Building, East Lansing, MI 48824; [email protected]

Catchweed bedstraw and wild mustard each produce two populations per year: a winter population (WP) in June, and a summer population (SP) in September. Experiments were conducted to determine whether the WP and SP differ in seed mass and seasonal germination. Seeds of both weeds were buried at 0, 5, 10, and 20 cm in cultivated fields, and retrieved at monthly intervals for 24 mo for germination tests in the laboratory. Additionally, seedling emergence from seeds buried at 0, 5, and 10 cm in the field was evaluated for 1 yr. Seeds from the WP were heavier than those from the SP for both species. Germination of exhumed seeds was affected by burial depth and by seed population. It was highest for seeds that remained on the soil surface and declined with increasing depth of burial. The WP of catchweed bedstraw produced two germination peaks per year, whereas the SP and all populations of wild mustard had only one peak. The WP of both weeds germinated earlier than the SP. Seedling emergence for both species in the field was greater for the WP than for the SP. Increasing soil depth reduced seedling emergence of both the WP and SP of wild mustard and affected only the WP of catchweed bedstraw. We conclude that the WP and SP of catchweed bedstraw and wild mustard seeds used in this study differed in seed mass, seasonal germination, and seedling emergence. The ability of a WP to produce large seeds that germinate early and have two germination peaks per year could make these populations a serious problem in cropping systems. Nomenclature: Catchweed bedstraw, Galium aparine L., GALAP; wild mustard, Brassica kaber (DC.) L.C. Wheeler. SINAR. Key words: Burial depth, dormancy, integrated weed management, mean emergence time, seed mass.

Catchweed bedstraw and wild mustard are aggressive weeds throughout most of the temperate regions of the world (Malik and Vanden Born 1988; Mennan 1998; Mennan and Isik 2003; Roebuck 1987; Schroeder et al. 1993; Wilson and Wright 1987). Both species produce many seeds with extended dormancy and cause considerable yield losses, especially in winter crops. In crop production systems, the soil seed bank is the primary source of new infestations of annual weeds such as catchweed bedstraw and wild mustard (Buhler et al. 1997). Studies on the germination biology of weeds are useful for development of long-term weed management strategies. To improve management systems for specific weed species, it is critical to have good information on seed dormancy, persistence, production, seasonal germination, seedling emergence, and variations among populations. Dormancy may be influenced by genetic, environmental, and biological factors (Baskin and Baskin 1998). Level of seed dormancy is influenced by temperature, amount and quality of irradiance, photoperiod, nutrition, and seed position during its development on the mother plant (Andersson and Milberg 1998; Baskin and Baskin 1995; Beckstead et al. 1996; Benech-Arnold et al. 2000; Fenner 1991; Gutterman 2000; Lord 1994; Milberg et al. 2000; Probert et al. 1985). Additionally, variation in dormancy level among weed populations is a well-known phenomenon (Andersson 114

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Weed Science 54, January–February 2006

and Milberg 1998; Milberg et al. 1996; Naylor and Abdalla 1982). Weed germination also differs among seeds collected in different years and from different mother plants (Andersson and Milberg 1998; Beckstead et al. 1996). Under the ecological conditions of Samsun, Turkey, both catchweed bedstraw and wild mustard have two main germination periods: March to May, and September to November. It is not known whether seeds produced from these different populations are morphologically different or exhibit differential viability, germination, and dormancy. Understanding these variations (if any) may help to develop more effective management systems. This could be achieved by putting more resources into the control of the most troublesome population or by favoring crop competitiveness (Benech-Arnold et al. 2000). Several studies on seed viability, seasonal germination, and emergence of seedlings from different depths of burial have been conducted on catchweed bedstraw and wild mus¨ zer tard (Malik and Vanden Born 1988; Mennan 2003; O 1972; Roebuck 1987). However, seasonal germination and emergence of seeds from populations that emerged at different seasons during the year has not been documented for either species. Therefore, our objective was to determine whether differences exist in seed mass, seasonal germination, and seedling emergence in populations of catchweed bedstraw and wild mustard that germinate at different seasons.

TABLE 1. Fresh seed mass (mean 6 SE) of winter (WP) and summer (SP) populations of catchweed bedstraw and wild mustard.a Winter population

Catchweed bedstraw Wild mustard

Summer population

Seed mass (mg seed21) 10.72 6 0.19 9.08 6 0.16 1.41 6 0.08 1.29 6 0.07

Significance (F test)

***b ***

a

Seeds for WP and SP were collected in June and September 2000, respectively. b *** P , 0.001.

Material and Methods

Seed Collection Seeds of catchweed bedstraw and wild mustard were collected from wheat (Triticum aestivum L.) and corn (Zea mays L.) fields in Samsun, Turkey, in June and September 2000. The June population is referred to as the winter population (WP) and the September population is referred to as the summer population (SP). Mature plants were harvested by hand, just before seed shedding. For each population, seeds from different plants were pooled and stored in plastic containers at room temperature until the beginning of the germination tests.

Seed Mass Average seed mass was determined by weighing 10 samples of 1,000 seeds from each population according to International Seed Testing Association (ISTA) rules (ISTA 1999).

Burial Experiment For each species and seed population, 500 seeds were wrapped with a plastic fabric and placed on the soil surface, or buried at 5, 10, or 20 cm in pots (diameter, 20 cm; height, 25 cm). Nylon mesh fabric was used to create conditions close to natural soil conditions (water, air, and, microorganism diffusion). The pots were filled with field soil without sterilization to maintain natural organisms. Soil was obtained from a depth of 50 cm to avoid the presence of other weed seeds. Textural composition of the soil was 27% sand, 28% silt, and 45% clay. It had an organic matter of 5.9%, and a pH of 6.7. The study used a completely randomized design with four replications for each seeding depth. A total of 384 pots were used for each weed species (4 depths, 24 exhumation times, and 4 replications). Pots were buried in a cultivated field at the end of September 2000. The seeds were about 105 and 30 d old for the WP and SP, respectively. Four replications from each depth of burial were exhumed from the field at monthly intervals (last day of the month) for 24 mo starting in October 2000. The seeds were cleaned in the laboratory before germination tests. Fifty intact seeds were selected and placed in 9-cmdiameter Petri dishes on two layers of filter paper that was moistened with 5 ml of distilled water. Catchweed bedstraw and wild mustard seeds were incubated in dark conditions at 10 and 15 C, respectively. These temperatures were found to be most suitable for germination of these species in previous studies (Boz 1997; Mennan 1998). Germinated seeds

TABLE 2. ANOVA results for effects of seed burial depth, exhumation date, and population on germination of catchweed bedstraw and wild mustard. Percentage germinationb

Source of variation

DFa

Catchweed bedstraw

Population Depth Month Population 3 depth Population 3 month Depth 3 month Population 3 depth 3 month

1 3 23 3 23 68 68

*** ** ** NS ** * *

a Degree of freedom. b Significance: P , 0.05

Wild mustard

*** ** ** NS * * *

(*), P , 0.01 (**), P , 0.001 (***), and NS

(non significant).

were counted and removed daily. Seeds with a radicle greater than 3 mm were considered germinated. Distilled water was added as needed to keep the filter paper moist. Germination tests were terminated after 14 d.

Seedling Emergence in the Field One hundred seeds of each population were sown in plastic pots (diameter, 20 cm; height, 25 cm) in September 2000. The same soil and seeds described above were used. The pots were buried in a cultivated field in a randomized complete block design with four replications. Seeding depths were 0, 5, and 10 cm. Seedling emergence in the field was monitored regularly. Seedlings were counted as emerged when the radicle was visible and removed after each count. Mean emergence time (MET) was calculated as: MET 5

O (n 3 d )/N

[1]

where n is the number of seedlings emerging per day, d is the number of days needed for emergence, and N is the total number of emerged seeds. Cumulative seedling emergence of both populations was monitored for 1 yr.

Statistical Analyses All data were arcsine transformed to improve homogeneity of variance, and each species was analyzed separately. Data on seed mass, germination percentage, and seedling emergence were analyzed by ANOVA followed by Tukey’s multiple range test to test differences between populations. All statistical analyses were conducted using SPSS (Version 12.0).

Results

Seed Mass There was a significant difference between WP and SP of both species (Table 1). For both species, seeds of WP were heavier than those of SP. For example, average seed mass for catchweed bedstraw was 10.72 (6 0.19) mg seed21 for the WP and 9.08 (6 0.16) mg seed21 for the SP. Similar results were found with wild mustard with seed of the WP being about 8.5% heavier than those of the SP. Mennan and Ngouajio: Weed seed germination

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FIGURE 1. Effect of different populations on seasonal germination of catchweed bedstraw. In September 2000, seeds for the winter population (WP) or the summer population (SP) were placed at the soil surface (A), or buried at 5 cm (B), 10 cm (C), or 20 cm (D) for a period ranging 1 to 24 mo before germination tests. Bars indicate standard errors of the mean. Seeds of the WP and the SP were collected in June 2000 and September 2000, respectively.

Burial Experiment The general pattern of seasonal germination of catchweed bedstraw and wild mustard seeds in the laboratory following burial at different depths and duration differed for the WP and the SP (P , 0.001). Results of ANOVA are summarized in Table 2. Significant differences were found between populations, depths, and months seeds were exhumed. For the WP of catchweed bedstraw, germination after 1 mo of burial was 48% for seed that remained at the soil surface (Figure 1). Seed germination declined with depth of burial to an average of 28% for seeds buried 20 cm. During subsequent months until February, germination of catchweed bedstraw declined regardless of the burial depth. Germination per116

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centage in the SP was very low from October to February when dormancy reached close to 90%. Seeds of catchweed bedstraw collected from the WP showed two peaks of germination per year. A major peak occurred at all burial depths in April–May and a minor peak in November. However, the SP had only one peak of germination per year. In general, the WP germinated earlier than the SP, a situation that mimics the germination period of mother plants for both populations. Seeds of wild mustard (both WP and SP) had low germination percentages in the first 4 to 5 mo of the experiment (Figure 2). Starting in March 2001, the proportion of germinating seeds increased gradually and reached their

FIGURE 2. Effect of different populations on the seasonal germination of wild mustard. Seeds of the winter population (WP) or summer population (SP) were placed at the soil surface (A), or buried at 5 cm (B), 10 cm (C), or 20 cm (D) for 1 to 24 mo before germination tests. Bars indicate standard errors of the mean. Seeds of the WP and SP were collected in June 2000 and in September 2000, respectively.

maximum in June for the WP and in August for the SP. Regardless of burial depth, germination of wild mustard showed one peak per year. The SP germinated to higher percentages than the WP at all burial depths. As observed with catchweed bedstraw, the WP germinated earlier than the SP. In addition to differences in germination time, the two populations responded differently to depth of seed burial. Maximum seed germination percentage was comparable for the WP and SP. However, greater total percentage of germination occurred for the SP when the seeds were buried.

Seedling Emergence in the Field Seedling emergence of catchweed bedstraw in the field was affected by burial depth and by seed population (Figure 3). Final percentage of seedling emergence in the field ranged from 84% to 44%, depending on depth of burial for the WP, and seedling emergence decreased with increasing seed burial depth. Emergence from each depth was significantly different from the other two in the WP. In contrast, the SP had a lower percentage of seedling emergence than the WP, and seed burial had no effect on emergence. Mennan and Ngouajio: Weed seed germination

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TABLE 3. Effect of seeding depth on mean emergence time (mean 6 SE) of catchweed bedstraw and wild mustard populations.a Seeding depth 0

5 cm

10 cm

Mean emergence time (d) Catchweed bedstraw WP SP Wild mustard WP SP

3.4 6 0.68 7.8 6 1.54 11.2 6 2.01 5.6 6 0.87 8.4 6 1.24 15.5 6 3.17 4.2 6 1.07 8.1 6 1.12 20.4 6 3.07 6.4 6 0.97 8.7 6 1.63 19.6 6 2.21

a Seeds for WP (winter populations) and SP (summer populations) were collected in June and September 2000, respectively.

FIGURE 3. Total seedling emergence of different populations of catchweed bedstraw and wild mustard seeds within 1 yr for the winter population (WP) and summer population (SP). Bars with same letters are not statistically different (P , 0.05). Seeds of the WP and SP were collected in June 2000 and in September 2000, respectively.

Seedling emergence of the WP and SP of wild mustard decreased with increasing burial depth (Figure 3). For both populations, seedling emergence was highly affected by burial depth. Seedlings of catchweed bedstraw WP began to emerge from the end of October until early December. Thereafter, it continued to emerge in low percentage from December to early March. Another significant peak of emergence occurred from mid-March to June. Seedling emergence of the SP began at the same time as the WP. However, seedling emergence percentage of the SP was initially 32% less than that of the WP. The SP reached maximum emergence in July. Wild mustard WPs and SPs have low initial germination percentages. The WP emerged about 2 to 3 wk earlier than the SP. After March, seedling emergence increased and reached a peak in May and July for the WP and SP, respectively. MET was affected by population in both species and was delayed as burial depth increased (Table 3). The MET of catchweed bedstraw populations was affected significantly. Differences in MET between wild mustard populations ranged from 4.2 to 20.4, depending on burial depth.

Discussion Significant differences in seed mass were found between the WP and the SP of both species. Environmental condi118

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tions that lead to shorter seed ripening periods often result in reduced seed mass and embryo nutrition during seed development. Differences in germination characteristics due to seed mass (Milberg et al. 1996; Paolini et al. 2001) or size of the mother plant (Philippi 1993) have been shown in different species. Catchweed bedstraw seed mass was shown to decrease when emergence of the mother plant was delayed during the growing season (Malik and Vanden Born 1988). Seed mass, germinability, and survival of wild mustard seeds have been shown to differ between years of production (Donald 1993). Seeds produced in drier soil were smaller and had negligible dormancy (Wright et al. 1999). In this perspective, seed mass could play a major role in allowing germination at a considerable distance below the soil surface (Benvenuti et al. 2001). Therefore, seed mass could be an important determinant of the composition of future seed banks. Even though both populations of the two species exhibited a typical annual seed dormancy/nondormancy cycle, differences were found in the seasonal germination response. This type of dormancy pattern has been found in several species (Banovetz and Scheiner 1994; Baskin and Baskin 1985, 1987; Baskin et al. 1992; Benvenuti et al. 2001; Chen and Kuo 1999; Honek et al. 1999; Mennan 2003; Omami et al. 1999; Van Assche et al. 2003). The differences in dormancy between populations may be genetic, but they could also be due to precipitation in the habitat, altitude, temperature, soil moisture, nutritional status of the mother plant, seed mass, and seed size (Andersson and Milberg 1998; Baskin and Baskin 1998; Meyer and Monsen 1992; Philippi 1993). Because seeds were collected at different times of the year, it is possible that they were adapted to the different ecological conditions under which they were produced. Seeds from different ecotypes, inflorescences of the same plant, portions of the same inflorescence, or even in different parts of the fruit can exhibit differential dormancy and germination (Gutterman 2000). This could be attributed to ecological adaptation or differences in weather (Andersson and Milberg 1998). On the other hand, dormancy of wild mustard is genetically determined by maternal control exerted by major genes related to seed mass, coat, and color (Garbutt and Witcombe 1986). These findings support our results that WPs and SPs of this species could have different levels of dormancy. Seeds of both species and populations on the soil surface germinated at higher percentages than those that were buried. Burial depth influenced the germination cycle through-

out the experiment, so that the shallowest seeds likely lost primary dormancy faster than deeper seeds. Fluctuating temperatures in the field probably helped break seed dormancy and promoted germination of nondormant seeds. These results agree with previous findings by Omami et al. (1999) on redroot pigweed (Amaranthus retroflexus L.), and by Mennan (2003) on catchweed bedstraw. Seedling emergence is known to be affected by the interaction among many factors, including weather conditions and soil characteristics (Benvenuti and Macchia 1997). However, seedling emergence behavior of seeds buried at increasing depths may also be linked to seed energy reserves. Differences in seed mass could explain at least part of population differences found in this study. The SP had smaller seed mass than the WP. Another possible explanation could be seed age. Seeds of the WP were about 75 d older than those of the SP. Germination of many weeds has been shown to increase with seed age (Colbach et al. 2002a, 2002b; ElKeblawy and Al-Ansari 2000; Qaderi et al. 2005). Low germination rates of fresh seed is due, for the most part, to primary dormancy, which normally disappears in about 2– 3 mo. Colbach et al. (2002a, 2002b) showed that when blackgrass (Alopecurus myosuroides Huds.) seeds of different ages are tested simultaneously, germination peaks of fresh seeds tend to lag behind those of older seeds. Similar results were found with Scotch thistle (Onopordum acanthium L.) (Qaderi et al. 2005). The results outlined above strongly suggest that the delay in germination of the SP of the species tested in this study could also be due to differences in seed age. However, the ability of the WP of catchweed bedstraw to exhibit two distinct peaks of germination is less likely to be due to seed age. Ecologically, variation in seed germination timing of different populations has been reported for many weed species (Meyer and Allen 1999). The variation in seedling emergence of the WP and the SP of catchweed bedstraw and wild mustard observed in this study is ecologically significant; the information could be used in integrated weed management programs to time sowing so that crop establishment is achieved before peak emergence of catchweed bedstraw or wild mustard. We conclude that the variations in seed mass and in seasonal germination from different depths of burial in catchweed bedstraw and wild mustard populations found in this study are ecologically meaningful. The period of seed production of both species showed ecologically significant variation in regulation of seed germination. In general, seeds of the WP of both species germinated and emerged earlier than those of the SP. Because of the delay in germination of the SP of both weeds, their competitive ability would be low. However, late emergence could allow these populations to escape control measures because most weed management strategies (especially herbicide applications) are implemented early in the season. Therefore, even though the SP might not cause any yield loss in a given year, it should be controlled as a part of integrated weed management programs to limit the size of the seedbank and future yield losses.

Acknowledgment We thank Dr. J. Masabni and the referees for their critical review of an early version of this manuscript.

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Received August 2, 2005, and approved October 13, 2005.