Flora characteristics of Chenier Wetland in Bohai Bay and biogeographic relations with adjacent wetlands

Abstract

A key step towards the restoration of heavily disturbed fragile coastal wetland ecosystems is determining the composition and characteristics of the plant communities involved. This study determined and characterized the community of higher plants in the Chenier wetland of Bohai Bay using a combination of field surveys, quadrat approaches, and multivariate statistical analyses. This community was then compared to other adjacent wetlands (Tianjin, Qinhuangdao, Laizhouwan, Jiaozhouwan, and Yellow River Delta wetland) located near the Huanghai and Bohai Seas using principal coordinate analysis (PCoA). Results showed a total of 56 higher plant species belonging to 52 genera from 20 families in Chenier wetland, the majority of which were dicotyledons. Single-species families were predominant, while larger families, including Gramineae, Compositae, Leguminosae, and Chenopodiaceae contained a higher number of species (each≥6 species). Cosmopolitan species were also dominant with apparent intrazonality. Abundance (number of species) of temperate species was twice that of tropical taxa. Species number of perennial herbs, such as Gramineae and Compositae, was generally higher. Plant diversity in the Chenier wetland, based on the Shannon-Wiener index, was observed to be between the Qinhuangdao and Laizhouwan indices, while no significant difference was found in other wetlands using the Simpson index. Despite these slight differences in diversity, PCoA based on species abundance and composition of the wetland flora suggest that the Bohai Chenier community was highly similar to the coastal wetlands in Tianjin and Laizhouwan, further suggesting that these two wetlands could be important breeding grounds and resources for the restoration of the plant ecosystem in the Chenier wetland.

Keywords

Bohai Bay / Chenier / coastal wetland / floristic geography / restoration

Introduction

Beach plants are important primary producers in coastal ecosystems. They are resilient and can survive harsh environmental conditions, such as dynamic changes of landforms (Bouzas et al., 2013), drought and limited freshwater supply (Mollema et al., 2013), nutrient deficiencies (Bermúdez and Retuerto, 2014a; Nzunda et al., 2014), shallow groundwater levels, and the implications of frequent ocean-land interactions (e.g., sea wind, waves, salt spray, erosion, and storm surges (Tanaka et al., 2011; Dobben and Slim, 2012; Fenu et al., 2013; Johnson et al., 2013; Johnsen et al., 2014). Not only do these plants support the food web of the entire coastal ecosystem, they also have great ecological value and crucial protective significance. The underground parts of plants (i.e., roots) can hold loose soil preventing erosion (Krauss et al., 2012), while the aboveground parts (i.e., branches and leaves) can reduce the impacts from wind and sand waves (Tanaka et al., 2011). Furthermore, above or underground parts) play a pivotal role in protecting the banks, promoting siltation, nourishing biodiversity, decomposing pollutants, lessening impacts of natural disasters, and protecting onshore infrastructures and human life (Tanaka et al., 2011; Fenu et al., 2013). However, due to tourism-related developments and exploitation of the beach area’s economically important derivatives (e.g., sand, oil, fish, salt), these ecosystems have been continuously disturbed by anthropogenic activities (Acosta et al., 2009; Reyes-Martínez et al., 2015). As a consequence, material and energy flows are frequently changed (Acosta et al., 2009; Reyes-Martínez et al., 2015). Degradation of landscapes and loss of vegetation have resulted in the extinction of some species, which has negatively affected various functions and the overall state of these ecosystems (Ciccarelli et al., 2012; Fenu et al., 2013).

The Chenier coast, located in the southwest region of Bohai Bay and mainly composed of shell fragments, is one of the few Chenier wetland ecosystems in the world that is still relatively intact. Thus, it has important scientific value in terms of studying the consequences of environmental changes (Wang et al., 2000a). However, human activities, such as increased tourism, oil exploration, salt and aquaculture pond construction, seashell-land-sand mining, and fishing have reduced the exportation of goods from the area by nearly 92.4% during the past 20 years (Tian et al., 2011). The environment suitable for plant survival continues to shrink or in some cases, has become extinct, resulting in dramatic decreases in species diversity. There is an urgent need then for plant protection and landscape reconstruction (Tian et al., 2011).

Over the past few decades, many studies have been carried out to better understand the formation (Wang et al., 2000a), distribution (Yue et al., 2012), environmental significance (Wang et al., 2000b) and matrix composition (Xia et al., 2013) of the Bohai Sea Coastal chenier. Xia et al. (2014) and Zhao et al. (2015a) reported the adaptability of different flora species specifically found in this area. Even so, several aspects of the community ecology and structure plant species in the area are still poorly understood. In addition, published reports on these topics are minimal , thus greatly hindering plant conservation and restoration work in the region (Xia et al., 2014; Zhang et al., 2014).

Composition and structure of plant assemblages are the basic properties of plant communities and the foundation of biodiversity (Liu et al., 2009). Flora is a general term used to refer to all plant species in a certain region, period, or vegetation type. Community taxonomic composition (e.g., families, genera, and species) and life-form characteristics, as well as their geographical distribution, could visually reflect responses to changing conditions. Temporal and spatial distribution also provide information that allow us to gain insights into the community’s and individual taxa’s history, geography, ecology, and system evolution (Zhang et al., 2009). Therefore, investigating a certain flora in a region not only clarifies the status of plant communities, but also provides insights as to the origin, migration, and distribution of plant groups (Wu et al., 2008; Xu et al., 2014).These are the very foundation on which the studies of plant diversity at different temporal and spatial scales are based (Liu et al., 2004). Floristic studies can also provide a wealth of information helpful for the protection of some plant resources against damages that may have been caused by human interference and thus better management of reserve areas (Mérigot et al., 2007; Volis and Blecher, 2010).

To better understand the vegetative characteristics and the origin of flora in the Chenier wetland, and thus enhance future efforts of habitat protection, recovery, and conservation, this study determined the higher plant community composition of the area and compared it to the other coastal wetland communities around the Bohai Sea Coast. Statistical analyses were then employed to link community composition to the key environmental drivers. These included characterizations of major species life forms, diversity, and abundance. Specifically, this study aimed to: (i) obtain basal information on the current compositional diversity of the wild higher plant species assemblage in the Bohai Sea coast Chenier wetland, and (ii) better understand the similarities of plant resources in the Chenier and the surrounding wetlands.

Materials and methods

Survey area

From mid-July to early August in 2013 and 2014, surveys were conducted in the Binzhou Chenier Island and Wetland National Nature Reserve, located on the southwest coast of Bohai Bay and north-east of Wudi County, respectively. The geographical coordinates were between 38°02′50.51″N and 38°21′06.06″N, 117°46′58.00″E and 118°05′42.95″E. The region is situated in an East Asian monsoon continental zone with a warm, semi-humid climate and four distinct seasons with both wet and dry periods. The annual average temperature was12.15±0.45°C, and precipitation ranged from 530 to 630 mm. Summer precipitation constituted 70% of the annual rainfall with multi-year evaporation of 2430.6 mm. The annual average wind speed was approximately 4.6 m/s (Tian et al., 2011). In addition, the freshwater resource in the area was scarce, mainly supplied by atmospheric precipitation and transit water. Tides were irregular semidiurnal, and storm surges could occur throughout the year (Li, 2013). The landform of the area was one of the rare Chenier coastal wetlands observed in the world, mainly characterized by a wide tidal flat with alternation of a broad coastal wetland and shell ridge. Notably, disturbance from human activities in the area were constant. Many areas had been developed into villages and tourism destinations (Zhao et al., 2011; Zhao et al., 2014). Invasive activities, such as coastal oil explorations, salt and agriculture pond construction, seashell and sand quarrying for porcelain crafts and manufacturing, and sea fishing were also present (Tian et al., 2011).

Within the vicinity of the Wangzi Island Reserve, the outcrop Chenier ridge was aligned and connected to the tidal flats on the seaside and the artificial wetland on the land side (Fig. 1). It was the largest outcrop Chenier wetland ecosystem currently existing (Zhao et al., 2015b).The area could only be accessed by seasonal fishermen from a small village populated by less than 20 people. Human activities in this area were relatively less compared to those on the other side of the coast. In addition, the reserve management had implemented measures such as closure to allow recovery of populations, resulting in higher plant diversity and abundance with a larger area of coverage. This area is representative of a typical undisturbed Chenier habitat with native vegetation, which is an ideal site for studying species vegetation, plant sources, and obtaining a better understanding of underlying ecological processes. For these reasons, the Wangzi Island area was chosen as a study region for detailed research and analysis of the higher plant composition.

Data collection and statistical analysis

The combination of field investigation and quadrat surveys was used to statistically analyze the plant species in the Wangzi Island area, Bohai Bay Chenier Island, and the Wetland National Nature Reserve. Field surveys were carried out during the growing season (May to October) from 2008‒2014, except for 2010. Plant species were recorded and summarized monthly. During the peak months of the growing season (around July to September) in 2013 and 2014, the combined methods of line transect and quadrats were used. The belt transects with 5 m width coverage, every 250‒300 m perpendicular to the coastline, were laid starting from the high tide line to the landside. Quadrats with sizes of 5 m × 5 m were set every 5 m. The shrub species in the belt transects and quadrats were recorded. In the quadrat, five sub-quadrats (1 m × 1 m) were set at diagonal positions, and the herbaceous plant species in the small quadrats were recorded and photographed, followed by the preservation of the specimens (Shen et al., 2011). A total of 9 line transects, 425 herb communities, and 85 shrub community quadrats were surveyed for the entire duration of the study.

Plants in the Chenier wetland were identified following descriptions provided in the “Flora of China” (http://frps.eflora.cn/) and “Flora of Shandong” (Chen et al., 1992, 1997). Plants were identified at species level, if applicable, and were then used as taxonomic groups for other statistical applications. The floristic geographical variables were classified according to the classification method suggested byWu (1991). The cosmopolitan compositions (T₁), tropic elements (T_trop), and temperate elements (T_temp) of families and genera were statistically analyzed. The T_trop included the distribution patterns of pan-tropical (T₂), tropical Asia and tropical American disjunction (T₃), old world tropical (T₄), tropical Asia to tropical Greater Asia (T₅), tropical Asia and tropical Africa (T₆), and tropical Asia (T₇). The T_temp meanwhile included the distribution patterns of northern temperate (T₈), eastern Asian and northern American disjunctions (T₉), old world temperate (T₁₀), temperate Asia (T₁₁), Mediterranean area, western Asia to central Asia (T₁₂), central Asia (T₁₃), and eastern Asia (T₁₄). Species frequency was calculated using the quadrat survey data. The geographical floral diversity index based on the genus was calculated using the Shannon-Wiener and Simpson indices (Liu et al., 2014):

(1)P_i={\displaystyle \frac{N_i}{N}},

(2)H={\displaystyle \sum _{T=\mathrm{1}}^M{Q}_T\ln Q_T},

(3)D=\mathrm{1}-{\displaystyle \sum _{T=\mathrm{1}}^M{Q}_T^{\mathrm{2}}},

where P_i was the occurrence frequency of species i and N was the total number of quadrats surveyed. In this study, the N for the shrub communities and the herb communities was 85 and 425, respectively. In addition,N_i was the quadrat number for species i. H and D represented the Shannon-Wiener diversity and Simpson index of the plant genera geographical flora, respectively. Q_T was the relative percentage of specific geographical floristic elements T in the total number of geographical flora M, which was equal to 14 in this area as mentioned above.

Principal coordinate analyses (PCoA) looked at the similarity of species distributions in the Bohai Sea coast, Chenier wetland, and adjacent wetlands, including Tianjin (TJ) (Mo et al., 2009), Qinhuangdao (QHD) (Zhang et al., 2004), Laizhouwan (LZW) (Zhang et al., 2008), Jiaozhouwan (JZW) (Zhang et al., 2006), and the coastal wetland in the Yellow River Delta (HHS) (Shao et al., 2002) and were carried out in Cannoco 4.5 (1982, Table 1). Other statistical tests were carried out in SPSS 19.0 and Excel 2007.

Results

A total of 56 wild, higher plant species belonging to 20 families and 52 genera were found in the Bohai Sea coast Chenier wetland for the entire duration of the study. Species found included 1 family, 1 genus, and 1 species ofGymnosperm, and 19 families, and 51 genera with 55 species belonging to Angiosperm. Within the Angiosperm group, 36 were dicotyledons and 19 monocotyledons, accounting for 64.29% and 33.93% of the total number of species and genus, respectively. The major plant families (in terms of abundance) were Gramineae, Compositae, Leguminosae, and Chenopodiaceae, totaling to 36 species in 34 genera. These groups alone accounted for 64.29% of the species and 65.38% of the total number of genus subgroups (Table 2, Fig. 2).

Dominance of single-species families was the main characteristic of the plant assemblage in the coast of the Chenier wetland where the 13 single-species families accounted for 65% of the total family number in this region. Species that belong to these families were 23.21% of the total species. Three families had 2–5 species each, which included Convolvulaceae (2 genera/2 species), Asclepiadaceae (2 genera/2 species), and Cyperaceae (1 genus/3 species). They consisted of 12.5% of the total number of species. On the other hand, 2 families had 6‒9 species, such as Chenopodiaceae (6 genera/6 species) and Leguminosae (6 genera/6 species), both accounting for 21.43% of the total species. Only Gramineae had more than 15 species, making up the majority of the species population at 26.79% (Fig. 3).

Smaller groups consisting of≤4 species were most characteristic of the coastal Chenier wetland. There were 49 monotypic genera, which accounted for 94.23% of the total number of genus and 87.5% of the total number of species. Cyprus had relatively more species with a total of 3 observed in this study (Fig. 2 and Fig. 3).Artemisia and Suaedahad 2 species each and 3 genera had 2‒3 species totaling 7 species, making up the minority of the population with 5.77% and 12.5% for both of the total number of genus and species, respectively.

Perennial herbs were the characteristic plant life-form, followed by annual or biennial plants, with the proportion of shrubs as the smallest (Fig. 4). In terms of type of distribution, plant families in the wetland were typically of the widespread type, followed by pan-tropically distributed groups. In addition to the cosmopolitan genera, species of a northern temperate distribution type occupied a relatively large proportion. Some species belonging to the tropical (12 genera) and temperate flora (12 genera) were also found. It was also observed that there were twice as many genera belonging to the temperate elements as those classified as tropical elements (Fig. 5).

Data on species frequency gathered by quadrat survey showed that the top two families were Gramineae and Compositae with occurrence frequencies of 77.67% and 74.76%, respectively (Table 3). In addition, the perennial plants were the most frequent (98%), followed by annual or biennial herbs (35.92%), and shrubs (24.27%, Fig. 4).

The Shannon-Wiener diversity indices of genus geographical flora at the coastal wetlands around the Yellow and Bohai Seas were significantly different. The Shannon diversity of genus geographical flora in the Bohai area was 1.954 which was in between that of Qinhuangdao (2.317) and Laizhou Bay coastal wetlands (1.842). However, diversity based on Simpson indices in these areas did not differ significantly (Fig. 6).

PCoA clustering based on floral abundances revealed that the PC1 accounted for the highest variations observed, contributing as much as 83.5%, while PC2 only accounted for 8.3% (Table 4). Furthermore, the clustering clearly showed that the six wetlands could be grouped into three categories, with the first being composed of Tianjin coastal wetland, Laizhou Bay, and the Bohai Sea coastal Chenier wetland. The Qinhuangdao coastal wetland and the Yellow River Delta wetland made up the second group, with the third composed of the coastal wetland of Jiaozhou Bay (Fig. 7).

Discussion

Coastal wetlands are considered to be among the most productive ecosystems that provide invaluable ecological services (Zhao et al., 2016). However, the loss or degradation of coastal wetlands, caused by naturally occurring harsh environment events and frequent human activities (Bai et al., 2015; Zhang et al., 2016) made the growth and survival of plants in these regions more challenging (Bai et al., 2014).Therefore, it is essential that the diversity of floral communities is protected and preserved, which would in turn promote the recovery and restoration efforts of damaged coastal wetlands (Priti et al., 2016). Coastal beach wetlands are narrow, isolated, and fragmented habitats that limit the population size, gene flow, and survival of plants. Reproduction meanwhile is strained by nature (Zhang et al., 2013). Many studies have shown that native wetland plants in coastal beaches or hills are relatively scarce (Benot et al., 2011; Estiarte et al., 2011). Field investigations and quadrat surveys from 2008 revealed the presence of 56 higher plant species in the Bohai Sea coastal Chenier wetland. However, previous studies based on surveys conducted from 1997‒1999 showed that there were around 350 higher plant species in the area, suggesting high species richness and diversity (Pan et al., 2001). However, the disparity in the number of species observed could be associated with the limited area that was covered in this study. Specifically, this study only surveyed the relatively largely exposed breakwater island area, potentially representing only a smaller proportion of the true species diversity. However, preliminary field surveys have also shown that due to human activities and coastal erosion, the Chenier wetland area has been dramatically shrinking in past years, which in turn could be contributing to the loss of diversity. Many smaller islands had disappeared, and the bigger breakwater islands were shrinking and were further exposed to erosion (Tian et al., 2011). On the other hand, the Wangzi Island area had a relatively larger outcrop and was well-preserved. The habitat and diversity status in Wangzi partly represented the current situation of the whole Chenier wetland plant communities. The species presented in the area only represents 16.0% of those found in the late 19^th to 20^th century. The disappearance of approximately 84.0% of the species is conceivable, which further supports the necessity for plant protection and recovery work in the area.

Beach plant species have adaptations to help them survive, reproduce, regenerate, and sustain these harsh conditions (Zinnert et al., 2012; Bermúdez and Retuerto, 2014b). Life forms and behavior are the external manifestations of plant adaptations to the environment, and are closely related to local climate/conditions. For example, perennial plants grow more rapidly in periods with favorable conditions and regenerate the population by asexual reproduction, thereby ensuring the survival of the species (Knevel and Lubke, 2004). Interestingly, we found that the Chenier wetland was dominated by perennial plants. In fact, Gramineae and Compositae species had the highest occurrence and abundance. Most of the species we observed had extensive growth of rhizomes and sprout, allowing and ensuring plant propagation and regeneration even after human or natural disturbance. This also allowed them to become the dominant plant taxa in the area.

Coastal wetlands dramatically change in habitat landscapes (Bai et al., 2014; Bai et al., 2015; Zhang et al., 2016), which also influences the distribution and composition of plants causing them to exhibit intrazonality (Wilton and Breitwieser, 2000; Peinado et al., 2007). By understanding species composition, this study has confirmed the non-zonal vegetative characteristics of the region. Plant species were mainly of worldwide distribution. At genus level, in addition to the cosmopolitan species distributed worldwide, temperate elements had the largest number of plant species, twice that of the tropical elements. This was consistent with the warm temperate climate conditions in the region. In addition, floral diversity at family and genus levels reflects the degree of variation in plant species, levels of evolution, and the diversity of life-forms adapted to different habitats. In this study, it was found that the diversity of plants in the level of the genus found in the Bohai Sea coastal Chenier wetland was high, indicating a higher degree of uniformity between genera and further suggesting non-prominence of the dominant species.

The biogeography of species will provide important baseline information for plant protection and reintroduction (Bai et al., 2014; Bontrager et al., 2014). Meanwhile, a plant dispersion model is a helpful tool to gain insights into the species’ biogeography (Lo et al., 2014). The special geographic location of the coastal beach ecosystem determines the variety of ways that plants spread and colonize new areas or habitats. Some of these characteristics are the capabilities for sexual or asexual reproduction, as well as the mechanisms for dispersal, which influences plant distribution in the region (Liu et al., 2014). The Chenier wetland was mainly dominated by native perennial herbs. Vegetative reproduction could then be an important way for adaptation to harsh habitats. Secondly, seawater movement generated by the ocean’s current may also be an important factor in spreading plant species, allowing them to invade new territories and spaces for population regeneration and proliferation (Tikka et al., 2001;Anastasia et al., 2011). Based on recent studies of the flora of Shandong province (Zhang and Zhao, 2002), the vegetation found in the southwest Bohai Sea Coast Chenier wetland belonged to the Holarctic Plant Zone, while the Lubei plain (Yellow River Delta) plant plot, and the wetland areas of Laizhou Bay and Yellow River Delta belonged to the Northern China Plain plant sub-region. However, the PCoA of the floristic characteristics of the species found showed significant similarities between the plant composition of those observed in the Bohai Sea Coast Chenier wetland and those in the coastal wetlands of Laizhouwan and Tianjin, whereas the similarities observed in the coastal wetlands of Jiaozhouwan, Yellow River Delta, and Qinhuangdao were significantly low. It is therefore strongly suggested that floating seeds could have been carried with the flow of ocean currents to thus facilitate a gene exchange between these adjacent regions. The gene exchange through seed dispersal resulted in highly similar gene pools in these areas, particularly for the plant species. Overall, results of this study showed that the coast wetlands in Laizhouwan and Tianjin could serve as important breeding grounds and seed banks for recovery of plant species in Chenier wetlands.

Conclusions

In this study, a total of 56 higher plant species in 52 genera from 20 families were found in Chenier wetland, the majority of which were dicotyledons. Single-species families and smaller groups with less than 4 species were the main distinguishing features. Cosmopolitan species strongly dominated with obvious intrazonality. The occurrence frequencies in quadrats of Gramineae, Compositae, and the perennial herbs were higher than for other families and life-form plants. Principal coordinate analysis of floristic geography showed that the plant composition of Chenier wetland was similar to that of the coastal wetlands at Tianjin and Laizhouwan. It is pivotal to consider the community characteristics of wild plants associated with Chenier habitats, especially in carrying out habitat restoration and protection efforts. In addition, it was important to consider Tianjin and Laizhouwan coastal wetlands as important breeding grounds and plant resources for the restoration of the plant ecosystem in the Chenier wetland in the future.

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