Background

In Korea, marshes of the east coast are not well developed, although those of the west coast are extensively developed (Ihm and Lee 1998). The west coast is the leading tideland characterized by large difference in ebb and flow of tides (about 8 m). Coastal wetlands such as salt marsh, salt swamp, and sand dune on the Korean Peninsula can be continuously found along the west coast. Because halophyte is developed in the upper intertidal zone, coastal wetlands have various ecological functions. They are ecotonal habitats with distinct ecosystems that connect both land and marine ecosystems. They provide important wildlife habitats for endangered species (Lee 2011; Lee et al. 2014a, b; Cho et al. 2017). They also increase biodiversity, decrease outer physical influence such as wave and current, and prevent coastal erosion (Kim et al. 2008; Lee 2011; Lee et al. 2014a, b). Pollutants from various wastewater of land can be adsorbed by salt marsh soil (Viles and Spencer 1995; Alhdad et al. 2015). In addition, pollutants can be purified naturally by animals, plants, and microorganisms inhabiting in the salt marsh soil (Lee and Yoon 1999; Park 1999; Kim et al. 2008; Lee et al. 2009; Lee 2011; Xie et al. 2017).

Zonation occurs in coastal wetlands of the southwestern coast. A wetland is an ideal habitat to study the relationship between distribution of species and environmental gradients (Lee et al. 2016). It is important to understand halophyte development and perform health assessment (Lee 2011; Lee et al. 2014a, b; Ivajnsic et al. 2016). When halophyte vegetation develops, the velocity of current flow will decrease and sediment will accumulate. Halophyte leaves dead bodies and roots in sediment layers to form new communities. Coastal wetlands have received attention recently due to their function in carbon sequestration and climate change adaptation (Cahoon et al. 1996; Rogel et al. 2000; Costa et al. 2003; Davidson-Amott et al. 2002; Kirwan and Guntenspergen 2012; Liu et al. 2015).

In South Korea, salt marshes have various vegetation distributions with high species diversity due to environmental gradients and zonations. Because salt marshes have been used for development purposes for several decades, distinct sediment geomorphology and marine species communities have been partially destroyed. Both quality and quantity of possible ecological services arising from the ecological function of salt marsh ecosystem have been deteriorated (Hong 2000; Maeng et al. 2007; Lee et al. 2014a, b).

Recently, researchers have attempted to restore salt marsh and estuary marsh (Chung and Park 1978; Ihm and Lee 1998; Glenn et al. 2006; Konisky et al. 2006: Nyman et al. 2006; Cho et al. 2017). To restore salt marsh and estuary marsh with balanced functions, the relationship between salt marsh halophyte communities and soil physico-chemical factors should be studied first. It is also important to identify appropriate methods to induce halophyte communities considering both environmental and biological factors.

Therefore, the objective of this study was to determine halophyte distribution in two types of soil (salt marsh and estuary marsh) in South Korea and analyze the relationship between halophyte distribution and soil environmental factors in the west coast of South Korea using canonical correspondence analysis (CCA) and germination rate analysis.

Results

Halophyte distribution

Of different study areas (Fig. 1), Yeongjong (S3) had the least diverse halophyte distribution with 4 families and 6 species, while Daebudo (S6) (9 families and 18 species) and Hyeonhwa (S13) (8 families and 19 species) had the most diverse halophyte distribution (Fig. 2). The latter two areas also had diverse soil environmental factors and complex topography (Fig. 3).

Fig. 3
figure 1

Box and whisker plots for environmental factors of soil in plant communities of salt marsh and estuary marsh at the 13 study sites (--- mean, ─ median)

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Fig. 1
figure 2

A map showing study sites including Suaeda japonica communities in the west coast of South Korea

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Fig. 7
figure 3

Suaeda maritima dead plants and seedlings having the same or similar with dead parental plants in estuary marsh at Gojan (S4) in January and April of 2004

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Habitat and soil environment factors

In this study, two vegetation groups (group 1 and group 2) were recognized (Fig. 4). Group 1 had distinct salt marsh vegetations, including Aster tripolium, Suaeda asparagoides, and Phacelurus latifolius. Salt and estuary marshes shared seven common vegetations: Phragmites communis, Carex scabrifolia, S. japonica, Triglochin maritimum, S. maritima, Salicornia herbaceae, and Limonium tetragonum. Group 2 had distinct estuary marsh vegetations, including Zoysia sinica, Calystegia soldanella, Artemisia fukudo, and Elymus mollis.

Fig. 2
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Number of species and family at the 13 study sites from July 2004 to August 2014

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Soil factors were analyzed for both salt marsh and estuary marshes (Fig. 1). For salt marsh and estuary marsh soils, pH values were 6.64 ± 0.42 and 6.95 ± 0.36, respectively. Moisture contents were 21.47 ± 8.02 and 25.45 ± 4.07%, respectively. Total organic carbon contents were 2.97 ± 1.74 and 4.27 ± 1.97%, respectively. Salinity values were 1.52 ± 0.92 and 1.23 ± 0.94, respectively. Electrical conductivity values were 2823.84 ± 1700.16 and 2312.07 ± 1604.10 μs, respectively. Total nitrogen contents were 0.31 ± 0.20 and 0.36 ± 0.21 mg/g, respectively. Average soil A-P contents were 158.05 ± 130.17 and 102.68 ± 122.77 μg/g, respectively. Gravel contents were 5.93 ± 8.32 and 0.09 ± 0.22%, respectively. Sand contents were 60.32 ± 23.25 and 39.71 ± 25.49%, respectively. Silt and clay contents in salt marsh were 21.69 ± 18.23 and 45.00 ± 15.29%, respectively. They were 12.16 ± 11.24 and 15.20 ± 16.61%, respectively, in estuary marsh. Altitude was 1.17 ± 1.32 m in salt marsh and 3.14 ± 1.33 m in estuary marsh. Therefore, soil pH, soil moisture, total organic carbon, total nitrogen, silt and clay contents, and altitude were higher in estuary marsh while soil salinity, electrical conductivity, soil A-P, gravel, and sand contents were higher in salt marsh.

Ordination

CCA ordination results of coastal wetland data set are shown in Fig. 4. A total of 14 community scores were plotted along axes 1 (Eigenvalue 0.021) and 2 (Eigenvalue 0.003). They tended to be clustered into two groups: the salt marsh group and the estuary marsh group. Based on correlation coefficients of environmental factors with the first CCA axis, axis 1 was highly correlated with gravel, silt, pH, and altitude while axis 2 was correlated with MC, TOC, and T-N (Table 1). In salt marshes, annual halophyte germinated in tidal level of the upper part of the coast line (Figs. 4, 5, and 6) while halophyte seedlings occurred in the same or similar altitude with dead parental plants (Fig. 6).

Table 1 Canonical coefficient and intraset correlation of salt marsh and estuary marsh for the 12 environmental factors
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Fig. 4
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CCA ordination diagram showing the relationship between plant species and soil properties of salt marsh and estuary marsh in the west coast of South Korea. Pc, Phragmites communis; Csc, Carex scabrifolia; Sj, Suaeda japonica; Tm, Triglochin maritimum; Zs, Zoysia sinica; Sm, Suaeda maritima; At, Aster tripolium; Sh, Salicornia herbaceae; Cso, Calystegia soldanella; Lt, Limonium tetragonum; Sa, Suaeda asparagoides; Pl, Phacelurus latifolius; Af, Artemisia fukudo; Em, Elymus mollis (S, salt marsh; E, estuary marsh)

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Fig. 5
figure 6

Sprout density of Suaeda japonica at germination time in salt marsh at Donggeom (S2) in April of 2004

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Discussion

Halophyte distribution

In the study area, Suaeda japonica, Carex scabrifolia, Triglochin maritimum, Phragmites communis, Limonium tetragonum, S. maritima, Salicornia herbaceae, Zoysia sinica, Artemisia fukudo, Elymus mollis, Calystegia soldanella, S. asparagoides, Phacelurus latifolius, and Aster tripolium were found (Figs. 1 and 7). Distinct zonation patterns occurred according to various soil characteristics and tidal levels (Figs. 4 and 5), consistent with previous reports (Lee 2011; Lee et al. 2016).

Fig. 6
figure 7

Germination area of Suaeda japonica lined with tidal level in salt marsh at

Donggeom (S2) in April of 2004

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Habitat characteristics and soil factors

Difference between salt marsh and estuary marsh might be due to geographical position and vegetation growth. The development of estuary marsh is related to sedimentation in rivers and tides (Viles and Spencer 1995; Park 2000; Oh and Bang 2003). Halophyte distribution patterns can change according to the development of sedimentation geomorphology and soil texture (Lee 2011; Ihm et al. 2007) as well as time duration of tidal flooding (Park 2008). Outer physical influence can also affect salt marsh sediment (Hong 2000; Korea Environment Institute 2006). Seed burial in the sediment or flow of dispersed seeds might have a larger effect on salt marsh than that on estuary marsh.

Ihm et al. (2007) and Cho et al. (2017) have recognized halophyte types as salt marsh, salt swamp, and sand dune in CCA and TWINSPAN classification based on species coverage. The salt marsh species group (group 2) in this study showed association with Artemisia scoparia, Aster tripolium, Atriplex gmelini, Limonium tetragonum, S. herbaceae, S. asparagoides, S. japonica, S. maritima, and Z. sinica. Salt-swamp species groups (groups 1 and 4) contained C. scabrifolia, P. communis, Scirpus fluviatilis, T. maritimum, and P. latifolius. Sand dune species group (group 3) showed association with Carex kobomugi, Messerschmidia sibirica, Carex pumila, E. mollis, Ischaemum anthephoroides, Ixeris repens, Lysimachia mauritiana, Salsola komarovi, and Vitex rotundifolia. After examining environmental correlates of species distribution within these three habitat types using DCA and CCA ordination results of coastal plant data set, Ihm et al. (2007) have shown similar ordination results.

Salt marsh communities in this study showed distribution along gravel and sand gradients while estuary marsh communities showed distribution along and soil factors such as TOC, silt, and MC (Fig. 4, Table 1). They tended to be clustered into the salt marsh group and new estuary marsh group. These results are consistent with previous results of halophyte distribution by salinity and soil texture (Cho et al. 2017), soil particle size on coastal dunes (Lee et al. 2007), soil factor gradient (Lee et al. 2009), and soil texture (Ihm et al. 2007; Kim et al. 2006). In a previous study for this region, a regression model has shown that the abundance of 14 coastal plant communities in salt marshes is dependent on soil pH, osmotic potential, and sand content (Ihm et al. 2006). In principal component analysis (PCA) of 12 soil properties (Ihm and Lee 1998), when 24 coastal plant communities were plotted in the space defined by the first two PCA axes, axes I and II accounted for 70 and 14% of total variances, respectively. In PCA, axis I was designated as a gradient for soil texture and water potential related to salinity. On PCA axis 1, coastal plant communities could be divided into the following three groups: (1) salt-marsh communities characterized by low water and osmotic potentials, high electrical conductivity, and elevated sodium and chloride contents; (2) salt swamp communities with moderate properties; and (3) sand dune communities with higher water and osmotic potentials but low sodium and chloride contents. These PCA results are consistent with conclusions drawn from our DCA and CCA.

As a result, halophyte distribution was affected by habitat characteristics such as soil physico-chemical factors and geomorphology. In this study, two habitat types had different environment characteristics factors. Soil factors were affected by outer physical influence such as tide level, tide current, and wave. Soil factor changes had a large effect on seed burial in sediment or flow of dispersed seeds.

Because seeds of S. japonica are small in size with low specific gravity, their seeds might have been flooded to the upper intertidal zone by flood tide. With a lower flow rate, more seeds might have established in flat geomorphology in Korea and Japan (Figs. 3, 4, 5, and 6; Wells et al. 1990; Alexander et al. 1991; Yokoishi and Tanimoto 1994; Min 2005; Sin and Kim 2010). Early germination rate was higher in the upper intertidal zone due to a higher seed sediment rate. After germination but before root development, seedlings could not establish. They can be withered due to root exposure to wave and current (Bird 1984; Choi 1993; Lee 2011; Gul et al. 2013). Therefore, early seedling establishment rate due to outer physical influence may determine individual maintenance, distribution range, and coverage of halophytes.

In salt marsh, seed germination rate was higher near dead parental plants with lower flood duration and frequency (buried seeds of Suaeda japonica 8954 (S2) and 2643 (S1) and seed germination rate 31.3m2 (S2) and 8.4m2 (S1)). As a result, seed germination was restricted due to lower effect of tide level and tidal current (Fig. 6; Harper 1977; Hubbel 1980; Okubo and Levin 1989; Willson 1992; Dalling et al. 1998; Min 2000, 2005).

Conclusions

Halophyte distribution is affected by soil factors and outer physical influence such as wave and current. Because estuary marsh has a narrower altitude range but higher average altitude than salt marsh, halophyte distribution is less affected by outer physical influence. To induce growth or restore the halophyte considering the effect of seawater and sediment movement in salt marsh, a growth-inducing method that can decrease outer physical influence related to wave and current is needed. In estuary marsh, it is important to prevent seed loss caused by waves at area with high plant density.

Methods

Study area and data collection

Halophyte communities in salt marshes (coastal wetlands that are regularly flooded by tides) and estuary marshes (coastal wetlands where seawater meets freshwater) were sampled from Dongmak-ri in Gwanghwa-do (S1) to Hyeonhwa-ri in Muan-gun (S13) (Fig. 1 and Appendix 1). A total of 13 sites and 18 plots in the west coast of South Korea (total distance, 290 km) were observed in this study. Coastal vegetation in these regions was monitored above 3 per community of each species. Except for S3 and S9, vegetation in all other sites were sampled from July 2004 to September 2014 and S3 from 2011 to 2012 and S9 in 2011. The relevé sampling method was performed using the phytosociological approach of Braun-Blanquet (1964). Dominance and sociability of all vascular plant species were included. The ecological gradient of plant communities was determined by the CCA ordination method.

By comparison of tidal elevation data in tidal station and altitude surveying data in intertidal zone, each altitude was determined in each community (from 2004 to 2014). To obtain topological conditions, Light Detection and Ranging Laser Radar (LiDAR) survey was conducted using Optech Ilris 36D. For leveling, MGL-3 DGPS was used.

Soil environment near roots was examined in five replicates at a depth of 15 cm (Fig. 3, Ihm and Lee 1998). Except for S4 and S9, soil in all other sites were sampled from July 2004 to September 2014, S4 from 2005 to 2009, and S9 in 2011. Air-dried samples were used for physico-chemical analysis. Moisture content (MC) was calculated as difference in weight between fresh soil and the same sample after oven-drying at 105 °C. Total organic carbon (TOC) was determined by ashing the sample at 550 °C for 4 h. Soil salinity, soil pH, and electrical conductivity of soil:water (1:5) extract were evaluated using a salinity meter (YSI 63, USA). Soil available phosphorus (A-P) content was measured at a wavelength of 880 nm using a spectrophotometer (APHA 1989). Total nitrogen (T-N) was determined by the micro-Kjeldahl method. Soil particle size was determined with a sieve according to the soil classification system (Ingram 1971; Folk 1954).

Data analysis

Distribution patterns of coastal plant communities were examined using the CCA method of Canoco program version 4.5 (ter Braak and Smilauer 2002).