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. 2004 Feb;93(2):119–125. doi: 10.1093/aob/mch018

Relationships Between Seed Germinability of Spergularia marina (Caryophyllaceae) and the Formation of Zonal Communities in an Inland Salt Marsh

CHRISTY T CARTER 1,*, IRWIN A UNGAR 1
PMCID: PMC4241073  PMID: 14672911

Abstract

• Background and Aims The formation of zonal communities may be attributed to differences in germination across the community and to timing of germination of seeds present in the seed bank. Our goals were two‐fold: (1) to assess the annual germination pattern of Spergularia marina; and (2) to determine whether germination of S. marina differed across zonal communities.

• Methods Fresh seeds were buried in an experimental garden in polyester bags. Bags were harvested monthly for 1 year and exposed to differing 12 h/12 h temperature regimes (5/15 °C, 5/25 °C, 15/25 °C and 20/35 °C) with a 12 h dark/12 h light photoperiod. Replicate seeds were exposed to 24 h dark. Seeds were also placed in different zonal communities to assess germinability in the field.

• Key Results Spergularia marina has a primary physiological dormancy. Conditional dormancy occurs from December to May and non‐dormancy from June to November. Field germination initiates in the spring when temperatures are cool and salinity is low due to flooding, and ceases in the summer when temperatures exceed germination requirements. Spergularia marina has a light requirement for germination.

• Conclusions If seeds become buried in the field or are light inhibited by Phragmites australis, they will remain dormant until they receive an adequate amount of light for germination. Since S. marina can germinate across all zones in a salt‐marsh community, the formation of zonal communities is not determined at the germination stage, but at some later stage of development.

Key words: Caryophyllaceae, halophyte, plant zonation, salt marsh, seed banks, seed dormancy, seed germination, Spergularia marina

INTRODUCTION

Zonation of plant species is a common feature of salt marshes worldwide (Ungar, 1974; Snow and Vince, 1984; Vince and Snow, 1984). Distribution of plants across inland, coastal, saline and non‐saline marshes, however, has been attributed to many different factors, both abiotic and biotic (Parker and Leck, 1985; Ungar, 1991). Even so, zonation within saline areas is a result of the tolerance limits of the plants growing in these areas and their competitive abilities. However, it is difficult to discern when, or if, competition is occurring between halophytic species in saline environments because salinity is a confounding factor, especially in hypersaline environments (Ungar, 1991). It is also unclear at which developmental stage zonation is initiated. Most studies have used mature plants and perennials to investigate zonation in salt marshes (Ungar et al., 1979; Snow and Vince, 1984; Vince and Snow, 1984; Bertness and Ellison, 1987; Bertness, 1991a). Ernst (1978), however, pointed out that plant distribution may not always be attributed to competition, but rather that the physiological tolerance of species at different stages of development could explain the discrepancy between fundamental and realized niches of a species.

Most studies conducted on plant zonation have been within perennial‐dominated coastal marshes or non‐saline marshes. Unlike inland salt marshes, the distribution of species in coastal systems is affected by tidal action and competition for light (Adams, 1963; Bertness and Ellison, 1987; Ellison, 1987; Bertness, 1991a, b; Bertness et al., 1992). The distribution of plants in freshwater marshes is driven by competition, inundation and draw‐down (van der Valk and Davis, 1978; Ungar, 1991).

Others have studied the influence of seed banks on zonational patterns within wetlands (van der Valk and Davis, 1978, 1979; Kadlec and Smith, 1984; Parker and Leck, 1985; Leck, 1989). Egler (1954) proposed in his Initial Floristics Composition model that the composition of the above‐ground vegetation during succession was influenced by the composition of the persistent seed bank. Since salt‐marsh seed banks tend to reflect entire floras of marsh communities instead of one particular zonal community within a marsh, the spatial and temporal distribution of species is directly related to the presence of persistent and transient seed banks and how these are affected by annual changes in salinity and flooding (Ungar, 2001). Seeds of Spergularia marina have been found in the seed bank across zonal communities in the Rittman, OH, salt marsh (Egan and Ungar, 2001), and maintain the largest persistent seed bank ever recorded in the literature for a flowering plant community, with a mean density of 471 135 seeds m–2 (Ungar, 1988).

For species with persistent seed banks, it is essential to understand the conditions under which seeds will or will not germinate. This includes investigating seed dormancy, alleviation of dormancy and whether or not dormancy can be re‐entered (Baskin and Baskin, 1998). Even though temperature requirements for germination may be known, little is known about the germination patterns of Spergularia marina over time (Ungar, 1991). Studies investigating seed dormancy would provide insight into the timing of germination and how this would relate to changes in above‐ground vegetation patterns, given the highly variable conditions of inland salt marshes, both spatially and temporally, and also into the recovery of sites after extreme environmental disturbance such as major flooding events.

The goal in this investigation was to address theories concerning whether the formation of zonal communities occurs at the germination stage of development. Using laboratory and field experiments, the following questions were asked: (a) How does burial affect germination of Spergularia marina? (b) Does germination change over time, indicating changing dormancies? (c) What are the optimal temperature and light conditions for the germination of these seeds? (d) Do seeds germinate differentially when placed across zonal communities in the field? (e) How do the environmental, or abiotic, factors fluctuate over the course of a year in an inland salt marsh?

MATERIALS AND METHODS

Site description

The study site is located on an abandoned salt‐mine well field on the property of the Morton Salt Company in Rittman, OH, USA (40°57′30′′N, 81°47′30′′W). The area is dominated by the annual halophytes Salicornia europaea, Atriplex prostrata and Spergularia marina. These halophytes form distinct zonal communities within the marsh, with S. europaea located nearest the unvegetated hypersaline pan followed by zones characterized by A. prostrata and S. marina. Because the marsh is a closed system, it is subjected to annual cycles of flooding in the late winter and spring, drying during the late summer and autumn, and freezing during the winter. Soil salinity readings vary greatly between the early spring and late summer, ranging from 0·07 % to 9·0 % total salts or greater, respectively (Ungar et al., 1979).

Description of species

Spergularia marina (L.) Griseb. is an annual with a cosmopolitan distribution and is found in coastal brackish and saline habitats of North America and inland along salted highways, salt marshes and alkaline areas (Gleason and Cronquist, 1991; Ungar, 1991). It grows to 35 cm in height and flowers from June through to September (Gleason and Cronquist, 1991), producing numerous capsules, that contain approx. 55 seeds, throughout its growing season (Ungar, 1988). Seeds are small, approx. 500 µm in diameter, and can be either winged or non‐winged (Gleason and Cronquist, 1991). Spergularia marina has been found growing in areas with concentrations up to 4·0 % total salts (Ungar, 1992), but seeds have been reported to germinate in NaCl concentrations of 1·0 % but not at 2·0 % under laboratory conditions (Keiffer and Ungar, 1997).

Seed source

Spergularia marina plants were collected from an inland salt marsh in Rittman, OH, during October 1998 for the dormancy cycle experiment. Plants were brought to the laboratory and allowed to air dry. Within 14 d, seeds were removed from dried plants and were placed in polyester mesh bags with each bag containing 25 seeds. A second set of seeds was collected on 22 Sept. 1999 for the zonation portion of this investigation. Seeds were also placed in polyester mesh bags with each containing 25 seeds.

Germination in the laboratory

A total of 384 polyester bags containing fresh S. marina seeds were buried in garden soil at a depth of at least 25 cm in 16‐cm‐diameter plastic pots with drainage holes. Each pot contained 16 bags. Pots were buried in the ground out of doors on the Ohio University campus in Athens, OH, in November of 1998, permitting natural exposure to rainfall and temperature fluctuations. The area was caged and a mesh shade cloth was secured to the soil surface on top of the pots to prevent disturbance. Two pots were randomly harvested monthly over a 12‐month period beginning in December 1998. Seeds from one pot were transferred from bags into 50 × 9 mm Gelman plastic Petri dishes containing two layers of Whatman no. 5 filter paper and 2 ml distilled water. Seeds from the second pot were transferred under green light into similar Petri dishes and were placed in metal cylinders to simulate 24 h dark. (Possible green light effects on germination were tested and none were found.)

A 2 × 4 × 12 factorial design was used to assess the effects of light, temperature and month, respectively, on the germination of Spergularia marina seeds. Four replicate Petri dishes each containing 25 seeds were placed in each of four alternating 12 h night/12 h day temperature regimes (5/15 °C, 5/25 °C, 15/25 °C and 20/35 °C) with a 12 h dark/12 h light photoperiod (20 µmol m–2 s–1) for 20 d. Replicates in metal containers were exposed to the same temperature regimes, but received 24 h dark for 20 d. Temperature regimes were selected to simulate seasonal temperature fluctuations in south‐east Ohio. A control of non‐buried fresh seed was also exposed to the same temperature and light treatments in November 1998, within 14 d of collection to ascertain whether Spergularia marina seeds have primary dormancy. Petri dishes were checked at 2‐d intervals for seed germination over the 20‐d period while those in metal containers were checked at the end of 20 d. Emergence of the radicle was the criterion used to assess seed germination.

Germination across zonal communities

A two‐way crossed‐effects model with blocking was used to test for effects of position (surface or buried) and zone on the germination of Spergularia marina seeds. A total of four blocks was used. Each block contained one 1 m2 plot in each of four vegetation zones (Salicornia europaea, Atriplex prostrata, Spergularia marina and Phragmites australis). Seeds were also placed into Phragmites australis plots where the vegetation had been removed to investigate increased light affects on germination. Within each vegetation and Phragmites‐removed zone, four mesh bags with 25 seeds each were placed on the surface and secured with a metal screen. Four additional bags were buried to a minimum depth of 10 cm. Bags were placed in the field on 17 Nov. 1999 and were harvested on 7 June 2000 following the natural stratification and germination period.

Environmental data

Environmental data for soil moisture, conductivity (used to determine percentage of salt) and pH were collected every 4–6 weeks beginning in September 1999 and ending in August 2000. The collection was extended beyond the length of time the seed bags were actually in the field to show the annual fluctuation in environmental parameters. Five soil cores, using a tulip bulb planter (6 cm diameter, with a circular area of 28·3 cm2 to a depth of 7·5 cm), were collected in each zone at five randomly selected established points. After collection, cores were returned to the laboratory and gravimetric soil moisture tests were immediately initiated following procedures outlined in Gardner (1986). Conductivity measurements were made on a 4 : 1 water : soil ratio with a Radiometer CDM 83 Conductivity Meter using a CDC304 electrode and pH readings were taken with an Radiometer ION 83 meter using a GK2401C combined electrode. The percentage of total salts was calculated from conductivity readings using conversions as suggested by Jackson (1958). Three sets of surface water depth measurements were collected in October, March and June at each of the five points in each zone.

Statistical analyses

For the laboratory investigation, percentage germination (mean ± s.e.) was calculated monthly for each temperature and photoperiod. A three‐way fixed‐effects general linear model (GLM) ANOVA with an α‐level of 0·05 using double precision was performed on arcsine square‐root transformed data to assess the effects of light, temperature and time on germination. However, less than 1·5 % of all seeds exposed to 24 h dark germinated for all months. Given the impossibility of meeting the equal variance requirement for ANOVA, this treatment was dropped from the analysis and a two‐way GLM ANOVA was performed for month and temperature on seeds exposed to 12 h light and 12 h dark. A Bonferroni post hoc test was used to compare individual means. Germination velocity (mean ± s.e.) was calculated for each temperature regime monthly using a modified Timson index, where 0 indicates that no seeds germinated and 100 indicates that all seeds germinated on the first day (Khan and Ungar, 1984). Data for both percentage of germination and germination velocity were subjected to a three‐way GLM ANOVA and a Bonferroni post hoc test was used to determine whether significant differences occurred between individual means.

For germination in zonal communities, final percentage germination (mean ± s.e.) was calculated for each plot. A two‐way fixed‐effects GLM ANOVA was performed on arcsine square‐root transformed data to assess the effects of position and zone on germination. Since block was considered a random effect, a custom model was selected instead of a full model to remove block from any interactions. An α‐level of 0·05 with double precision was used. A Bonferroni post hoc test was used to compare individual means.

Environmental data for percentage soil moisture, percentage total salts and pH were transformed to meet equal variance and normality assumptions of ANOVA. Data for water depth were also transformed to meet normality assumptions, yet failed to meet the equal variance assumption. Since ANOVA is a robust test and can withstand departures from homogeneity, data for water depth were subjected to an ANOVA (Dowdy and Wearden, 1991). Each was analysed using a two‐way fixed‐effects GLM ANOVA with an α‐level of 0·05 with double precision to test the effects of zone and month. A Bonferroni post hoc test was used to compare individual means when significant differences were found among zones and months. All statistical analyses were performed in NCSS 2001 (Hintze, 2001).

RESULTS

Germination in the laboratory

Six per cent of freshly collected seeds germinated in the 5/15 °C temperature regime in the light treatment, whereas none germinated in the remaining three temperature regimes (Fig. 1A). No freshly collected seeds germinated in the dark treatment for all temperature regimes. Less than 8 % of seeds exposed to 24 h dark germinated for any given month except for the 5/15 °C treatment in November, which had germination of approx. 30 % (Fig. 1B). A significant two‐way interaction was found for month and temperature for percentage germination (F =10·53; P < 0·01; Power = 1·0) (Fig. 1A), with seeds demonstrating the greatest overall germination at 5/15 °C and the least at 20/35 °C (Fig. 1A). A significant two‐way interaction was also found for month and temperature for rate of germination (F = 20·92; P < 0·01; Power = 1·0). The greatest rates of germination were found in the 5/15 °C temperature regime in the spring months and 15/25 °C temperature regime in the summer months, and the least were found in the 20/35 °C temperature regime.

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Fig. 1. Percentage germination (mean ± s.e.) of Spergularia marina seeds harvested monthly and for fresh seeds (C = fresh seed control) in four alternating temperature regimes. A, Exposed to alternating 12 h light/12 h dark treatments; B, exposed to 24 h dark treatments for 20 d.

Germination in zonal communities

Less than 1·2 % of buried seeds germinated across all plots. Because the equal variance assumption of ANOVA was not met, the dark treatment was dropped from the analysis and instead a one‐way fixed‐effects ANOVA with blocking was performed to assess germination differences among zones for seeds placed on the surface. There was a significant zone effect (F = 8·21; P < 0·01; Power = 0·997) and a significant block effect (F = 10·40; P < 0·01). A significant block effect for germination in the field can be attributed to one plot (in one block) in the Phragmites‐covered treatment. When bags of seeds were placed in the field in the covered Phragmites treatment, they were placed on top of Phragmites leaf litter, not underneath. Over the course of the winter, bags of seeds within this one plot became covered with leaf litter and so were shaded during the spring germination period. Germination percentages from this plot were significantly lower than in other plots within the same zone. After reviewing the data, the analysis was run a second time using only three blocks. No significant block effect (F = 2·16; P > 0·05) was found but there was a significant zone effect (F = 3·54; P < 0·05; Power = 0·83) (Table 1).

Table 1.

Percentage germination (mean ± s.e.) of seeds of Spergularia marina in zonal communities in the field

Zone Germination (%)
Salicornia europaea 100·0 ± 0·0a
Atriplex prostrata 100·0 ± 0·0a
Spergularia marina 99·0 ± 0·72ab
Phragmites australis (removed) 94·3 ± 2·63b
Phragmites australis (covered) 97·0 ± 2·04ab
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Different superscript letters indicate significant differences (P = 0·05) in germination between zones based on a Bonferroni post hoc test.

Values for percentage germination were calculated based on data from three blocks.

Environmental data

A significant interaction of month and zone was found for percentage soil moisture (F = 3·02; P < 0·01; Power = 0·99) (Fig. 2A). For percentage of total salts, month (F = 60·84; P < 0·01; Power = 1·0) and zone (F = 115·73; P < 0·01; Power = 1·0) were both significant, but no significant interaction was found (F = 1·32; P > 0·05; Power = 1·0) (Fig. 2B). Both month (F = 5·37; P < 0·01; Power = 0·99) and zone (F = 31·0; P < 0·01; Power = 1·0) for pH were significant, but no significant interaction was found (F = 1·36; P > 0·05; Power = 0·98) (Fig. 2C). A significant interaction of month and zone was found for water depth (F = 6·08; P < 0·05; Power = 0·99) (Fig. 2D).

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Fig. 2. Environmental data (mean ± s.e.) from different zones on the Rittman, OH, salt marsh. A, Percentage soil moisture; B, percentage total salts; C, pH; D, water depth. SE, Salicornia europaea zone; AP, Atriplex prostrata zone; SM, Spergularia marina zone; PR, Phragmites australis‐removed treatment; PC, Phragmites australis‐covered treatment.

DISCUSSION

Germination in the laboratory

Spergulariamarina seeds have a primary innate dormancy as indicated by the lack of germination of fresh seeds. This is followed by a period of conditional dormancy from December through to May where seeds increase in germination over a period of time when they are exposed to cold stratification. Seeds are non‐dormant from June to November. These findings are consistent with those of Ungar (1984) who, under laboratory conditions, found that germination percentages of S. marina were the greatest after 4 weeks of cold stratification in a 5/15 °C night/day temperature regime. This is the first case of conditional dormancy reported for a salt‐marsh species (Baskin and Baskin, 1998).

Seeds are produced on plants throughout the summer growing season when salinity within the marsh and daily temperatures are at their highest. These data show that seeds of S. marina demonstrated the least germination in the summer temperature regime of 20/35 °C across all months and the greatest germination was at the early spring temperature of 5/15 °C. The 20/35 °C temperature regime was outside of the temperature range to promote germination for this species. At the onset of warmer summer temperatures, this species will not germinate in the field throughout the summer months. This species has also been observed to germinate in the field late in the autumn when temperatures have cooled and salinity in the marsh has been reduced due to flooding, but these germinating seeds are most likely from the previous year’s growing season since newly produced seeds need cold stratification to germinate. The ability to germinate in all temperature regimes was greatest in June and July and was lowest from December to February. Unlike some species with primary physiological dormancy and a persistent seed bank, S. marina does not appear to enter secondary dormancy. However, the experiment was not conducted long enough to make this determination.

In addition to percentage germination, data for rates of germination are useful in providing information about the suitability of germination conditions (Baskin and Baskin, 1998). The data given here indicate that the rate of germination for seeds of Spergularia marina closely follows their germination pattern. This permits species the best opportunity to take advantage of optimal germination conditions. From an ecological perspective, physiological dormancy ensures that seeds will germinate under conditions that are optimal for germination and growth – conditions that approximate spring and autumn temperatures when the salinity in the marsh is at its lowest.

In the dark treatment, germination increased to 30 % in November for the 5/15 °C temperature regime. In some cases temperature is able to overcome the light requirement of a species, in that it may be light‐requiring at one temperature but not necessarily at another (Pons, 2000). Unfortunately, only enough seed was buried for 12 months of collection. It is evident that seeds of Spergularia marina have a strict light requirement for germination given that few seeds germinated that were either buried in different zones in the field or exposed to 24 h dark in the laboratory. Having a light requirement for germination ensures seeds have enough available reserves for the shoot to reach the soil surface (Pons, 2000). Another benefit of having a light requirement is the formation of a persistent seed bank in the dark. The light requirement, often associated with small seeds (Thompson and Grime, 1979; Thompson, 1987), permits development of a large persistent seed bank when seeds are buried (471 135 seeds m–2; Ungar, 1988).

Germination in zonal communities

Germination of S. marina among the three zones of halophytic annuals was not significantly different even though differences did occur between the Phragmites‐cleared treatment and the Salicornia europaea and Atriplex prostrata zones. The realized niche of Spergularia marina, therefore, is not due to its response at the germination stage in the field, because seeds at the soil surface do germinate within the Salicornia europaea and Atriplex prostrata zones. This can be explained by the timing of germination in spring when the reduced salinity of all marsh zones containing the dominant annual halophytes is approx. 0·5 %. Because of the reduced salinity in all zones during the spring, environmental conditions cannot be considered inhibitory to germination of S. marina in the zonal communities. There were, however, interesting patterns across months for all environmental data collected. Soil moisture and water depth were lowest in September when the percentage of total salts was greatest. These conditions were reversed during spring when the marsh was flooded. Readings for pH for all months and zones were between 5·5 and 7·2. Light (or burial) and alleviation of salinity stress were the defining factors for determining the germination response of this species in the field. Our findings differ from van der Valk and Davis (1978) who found that water depth was significant in determining which seeds germinate in prairie glacial marsh seed banks. Since S. marina is found in the seed bank of all zonal communities in this marsh and is capable of germinating in each of these zones, other factors such as salt tolerance or flooding at the seedling or mature plant stages of development will have to be studied to determine how they influence zonation of Spergularia marina.

Significant differences did occur between the Phragmites cleared treatment and the two annual halophyte zones of Salicornia europaea and Atriplex prostrata. This is most likely due to a shading effect of surrounding Phragmites australis, accumulated leaf litter and a build‐up of silt covering the bags during the flooding season. Although significantly different, percentage germination for the Phragmites cleared treatment was still above 90. Because both the above‐ground vegetation and leaf litter were removed in this treatment, this may have created a situation that made it easier for bags of seeds to become ‘buried’ by floating leaf material and clay soil deposits when flooding occurred. It had been expected that seeds placed in the Phragmites covered treatment would also have lower germination percentages like the Phragmites‐cleared treatment, but found that this treatment did not significantly differ from the three zones dominated by annual halophytes. This can be attributed to the fact that bags were placed on top of the P. australis leaf litter and not underneath, thereby receiving an adequate amount of light for germination. Under natural conditions, small seeds of S. marina would sometimes fall underneath the leaf litter and become buried. Even though S. marina can germinate underneath P. australis, it may not receive an adequate amount of light at the seedling stage of development, given that P. australis occurs as a dense monotypic stand. As P. australis spreads vegetatively throughout the salt marsh, it will eventually replace S. marina in the above‐ground vegetation and the persistence of S. marina will be determined by the viability of its persistent seed bank.

The germination patterns associated with S. marina indicate that it has a primary dormancy, followed by a period of conditional dormancy from December to May, and non‐dormancy from June to November. When produced in the summer and early autumn, seeds will remain dormant until they receive a period of cold stratification. In the field, germination will occur in the early spring when temperatures are cool and salinity in the marsh is low due to flooding, and will cease in the summer months when temperatures are too high. Similarly, if a flooding event or some other environmental catastrophe occurred during the summer months, the zonal communities once dominated by S. marina would be replaced with other annual marsh species given the inability of S. marina to germinate at warm summer temperatures. Spergularia marina has a light requirement for germination. If seeds become buried in the soil in the field or are light‐inhibited by Phragmites australis, they will remain in the soil until they receive an adequate amount of light for germination. Since S. marina can germinate across all zones in a salt‐marsh community, the formation of zonal communities is not determined at the germination stage, but at some later stage of development.

ACKNOWLEDGEMENTS

The authors thank Carolyn Reilly and Dr Todd P. Egan for assistance with seed counting and Harold Blazier for providing glasshouse space. We are also grateful to two anonymous reviewers who provided helpful and thought‐provoking comments. This study was financially supported by the Ohio University Research Challenge Grant to I.A.U.

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Received: 13 June 2003; Returned for revision: 3 September 2003; Accepted: 3 October 2003:    Published electronically: 12 December 2003

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Articles from Annals of Botany are provided here courtesy of Oxford University Press

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