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Effect of Saltmarsh Cordgrass Spartina alterniflora Invasion Stage on Cerithidea cingulata (Caenogastropoda: Potamididae) Distribution: A Case Study from a Tidal Flat of Western Pacific Ocean China.

Byline: Bao-Ming Ge Dai-Zhen Zhang Yi-Xin Bao Jun Cui Bo-Ping Tang and Zhi-Yuan Hu

Abstract The effect of saltmarsh cordgrass Spartina alterniflora (Poales: Poaceae) invasion stage on Cerithidea cingulata (Caenogastropoda: Potamididae) distribution was studied in 2007 at the eastern tidal flat of Lingkun Island Wenzhou Bay China. The distribution pattern of C. cingulata was aggregated during each season as shown in experiments utilizing Taylor's power regression and Iowa's patchiness regression methods (P less than 0.001). Two- way ANOVA indicated that densities were significantly affected by S. alterniflora invasion stage (P less than 0.001) however no significant season effect was found (P = 0.090) and on the interaction between the seasons (P = 0.939). The density distribution during the invasion stage was significantly different in each season as shown in one-way ANOVA. Pearson's correlation coefficient analysis of density data indicated that the highest densities occurred in habitats at the initial invasion stage during summer.

The peak in C. cingulata density during spring autumn and winter occurred in habitats where invasion was classified as initial whereas the lowest densities occurred in the stage of invasion completed during each season. C. cingulata density distribution varied among different habitats and such variation indicates the response of the species to environmental change particularly S. alterniflora invasion.

Key words: Coastal wetland distribution pattern ecosystem engineer gastropod Wenzhou Bay INTRODUCTION

Gastropods serve an important function in the habitat and ecosystem of a tidal flat; gastropods are important foragers in the benthic community and environment (Anderson and Underwood 1997). Predatory snails can consume competitively dominant species to increase diversity in the community; such snails create sufficient space for colonisation by competitively inferior organisms such as Nucella spp. (Menge et al. 1994). Cerithidea cingulata (Gmelin) (Caenogastropoda: Potamididae) is a gastropod that is distributed worldwide particularly along the coasts of the Western Pacific Ocean Indian Ocean and Persian Gulf (Al-Kandari et al. 2000; Zheng et al. 2007; Reid et al. 2008). People consume C. cingulata as food but this species is also a pest snail" competing food and space with commercially important molluscs such as Bullacta exarata

Moerella iridescens and Tegillarca granosa farmed in aquaculture in coastal areas (Bagarinao and Lantin-Olaguer. 2000; Zheng et al. 2007). C. cingulata is also widely distributed in the tidal flats of Jiangsu Shanghai Zhejiang and Fujian China.

In recent decades salt-adapted grasses of the genus Spartina (cordgrass) have invaded western Pacific coasts including those of Japan and China (Greenberg et al. 2006). Many species of genus Spartina (cordgrass) are highly invasive (Daehler and Strong 1996). Cordgrass is a key ecosystem engineer in a salt marsh ecosystem (Pennings and Bertness 2001; Brusati and Grosholz 2006) and its occurrence could significantly change the benthic community structure (Hedge and Kriwoken 2000; Neira et al. 2006). Spartina alterniflora Loisel. (Poales: Poaceae) commonly known as saltmarsh cordgrass is a perennial salt marsh grass that is native to the Atlantic and Gulf coasts of North America; this species has extensively invaded the coasts of the Western Pacific Ocean and has affected native ecosystems particularly in China (Wang et al. 2006; Yuan et al. 2013).

In coastal wetlands invasive plants are ecosystem engineers that can change water flow light and sediments and can affect benthic communities (Neira et al. 2007). Ecosystem engineers are species that can create maintain modify or destroy the habitat of benthos thereby strongly influencing community composition and structure (Jones et al. 1994). When an invasive plant (an ecosystem engineer) colonizes a coastal wetland the community structure and the entire ecosystem are modified because nutrient cycling productivity hydrology particle flux and habitat availability are altered (Talley and Levin 2001; Crooks 2002).

S. alterniflora may outcompete native plants threaten the native ecosystem and coastal aquaculture and reduce native species richness (Neira et al. 2005; Levin et al. 2006). However the decline or increase in biodiversity in a wetland ecosystem because of S. alterniflora invasion is a highly controversial topic previous studies have shown that depending on conditions invasion can lead to either a decline or increase in biodiversity (Wang et al. 2010; Alphin and Posey 2000). A literature search has indicated that information is lacking on gastropod distribution in tidal flat patches at different stages of S. alterniflora invasion (Neira et al. 2007). C. cingulata is widely distributed on the tidal flats of Jiangsu Shanghai Zhejiang and Fujian China a region subject to ongoing colonisation by S. alterniflora.

In the current study we hypothesized that the C. cingulata population showed different distribution characteristics in the tidal flat at different S. alterniflora invasion stages such that the plant was influencing the distribution of C. cingulata.

MATERIALS AND METHODS

Study area and sampling protocol

Our study was conducted at the eastern tidal flat of Lingkun Island (N 27.95 E 120.93) Wenzhou Bay Zhejiang province China. This island is located in the estuary of Oujiang River which is characterized by a subtropical climate. The average salinity of the seawater in the tidal flat is 16 psu and the tide type is informal semidiurnal with an average tidal range of 4.5 m (Lu et al. 2005; Ge et al. 2011). The soft sediment is mainly silt. In 1989 S. alterniflora was deliberately introduced along the eastern tidal flats of Lingkun Island to promote sediment deposition (Li et al. 2009) and by 2007 had become the dominant plant in the upper and high tidal zones.

Five habitats were selected based on similar environmental characteristics (e.g. climate and salinity) (Fig. 1). In the high tidal zone four kinds of patches of S. alterniflora at different invasion stages were categorised based on invasion age of S. alternifloranamely; (1) no invasion (2) initial invasion (invasion age 1-2 years) (3) invasion underway (invasion age 3-4 years) and (4) invasion completed (invasion age 5-6 years) (Table I). A parallel habitat was selected as a negative control plot in the middle tidal zone and termed as (0) naked mud flat.

The site was sampled in February (winter) May (spring) August (summer) and November (autumn) of 2007. The habitats were 200-300 m apart replicated five times with plots (1 m A- 1 m) randomly sampled within each habitat and at least 2 m apart. A wooden quadrat was used to delimitate the plots and C. cingulata with a body length of greater than 0.5 cm collected by hand from within each quadrat. Each season 25 plots were sampled with a total of 100 samples collected for analysis.

Data multivariate analyses

For point pattern processes indices were obtained mainly based on counts of individuals per unit grid (quadrat). The simplest indices were based on variance (S2) and mean density (x) or on mean crowding (m) and mean density (x) of population

Table I.- Sample habitats with different S. alterniflora invasion stages within the eastern Lingkun Island tidal zone.

Habitat###Tidal###Invaded

###Coverage and area###

code###zone###years

0###Middle###Bare###0

1###High###Bare###0

2###High###About 10% (in winter) -###1-2

###30 % (in summer) about

###15 m2###

3###High###About 40% (in winter) -###3-4

###70 % (in summer) about

###50 m2

4###High###About 70% (in winter) -###5-6

###100 % (in summer)

###larger than 100 m2

density per quadrat. Taylor's power regression ln S2 = a + blnx (Taylor 1961) and Iowa's patchiness regression m = a + AYx (Iwao 1968) facilitated the assessment of the level of aggregation by means of slope b and AY. Taylor's law is an empirical law in ecology that relates the between-sample variance in density to the overall mean density of a sample of organisms in a study area. In Taylor's power regression the slope values (b) significantly greater than 1 indicate clumping of the organisms. In Poisson distributed data b = 1. If the population follows a lognormal or gamma distribution then b = 2. Iowa's patchiness regression where a indicates the tendency to crowding (positive) or repulsion (negative) and AY reflects the distribution of population on space and is interpreted in the same manner as b of Taylor's power. Such assessment indicated uniform [b(AY) less than 1] random [b(AY) = 1] or aggregated [b(AY) greater than 1] distributions of the population (Arnaldo and Torres 2005; Vinatier et al. 2011).

Two-way ANOVA (general linear model GLM) was used to determine the mean differences in density by distance season and interaction between the seasons; Levene's test was used to determine equality of variance before using the GLM and all the data sets passed this test in the current study (Ge et al. 2011).

One-way ANOVA was used to determine the significance of differences in density measured in plots in each season and StudentNewmanKeuls (SNK) method used if a significant difference occurred for multiple comparisons. Levene's test was used to determine equality of variance prior to the multiple comparison analyses. When a dataset failed to pass Levene's test the data was transformed using ln(x + 1) (Kendrick and Walker 1995). The data sets of mean densities in different habitats were then checked by Pearson's correlation coefficients among seasons.

SPSS 16.0 (SPSS Inc.) and Microsoft Office Excel 2003 (Microsoft Inc.) were used for statistical analysis.

RESULTS

Our results indicated that b and AY was slightly greater than 1 totally (P less than 0.001) and Iowa's model fitted the data better than Taylor's power law (Table II). In Iowa's model a less than 0 indicates the tendency to repulsion and indicates C. cingulata was aggregated in each season under the spatial scale of this study. Two-way ANOVA revealed a significant effect of plant invasion stage (F419 = 14.397 P less than 0.001) on the abundance of C. cingulata but no significant effect of season (F319 = 2.235 P = 0.090) and interaction of season A- invasion stage (F1219 = 0.447 P = 0. 939) was observed.

C. cingulata showed a clumped distribution in the habitats with no invasion and with initial invasion of S. alterniflora in the high tidal zone of Lingkun Island. Significant difference in the C. cingulata density across seasons were detected (SNK test Fig. 2). The highest density occurred in habitats at the initial S. alterniflora invasion stage in spring autumn and winter and in the habitat with no invasion in summer (Fig. 2). Patches with completed invasion had the lowest density (Fig. 2).

The density in naked mud flat in the middle tidal zone showed a medium value in each season. Significantly positive correlations on abundance distribution occurred in spring vs. winter (P = 0.030) spring vs. summer (P = 0.028) autumn vs. spring (P=0.002) and autumn vs. summer (P = 0.018) according to Pearson's correlation test for density distribution among seasons (Table III). The results showed that the number composition of density distribution at different habitats varied significantly in the mentioned comparisons.

Table II.-###Estimated values of C. cingulate dispersion indexes based on Taylor's power law and Iowa's patchiness regression.

Season###Taylor's power regression###Iowa's patchiness regression

###a###b###R2###P###R2###P

Winter###-0.878###1.525###0.658###0.048###-0.330###1.077###0.965###0.001

Spring###-0307###1.355###0.805###0.019###-0.085###1.064###0.988###less than 0.001

Summer###-0.989###1.573###0.971###0.001###-0.430###1.080###0.998###less than 0.001

Autumn###-1.311###1.662###0.869###0.007###-0.595###1.084###0.993###less than 0.001

Total###-0.990###1.568###0.830###less than 0.001###-0.439###1.083###0.990###less than 0.001

DISCUSSION

Previous studies have shown that some gastropod species showed an aggregated spatial distribution pattern (Ye and Lu 2001; Ge et al. 2013). A similar result was observed in the current research. Significant seasonal differences in C. cingulata densities were observed; however previous research has indicated that density variation can affect the distribution pattern (Hanberry et al. 2011) as spatial disposition can be the variation in C. cingulata densities observed in this study did not significantly impact on the underlying distribution pattern.

The comparisons of spatial distribution across seasons showed that higher densities of C. cingulata occurred at the no invasion and initial invasion patches in each season whereas the lowest densities occurred in patches where invasion was completed. Different invasion statuses can lead to alterations in litter production belowground biomass sediment organic content and nutrient cycling (Talley and Levin 2001) and such features are associated with food availability for benthic fauna (Neira et al. 2005). The trophic function of the wetland is also affected (Levin et al. 2006). The distribution of bethos could be affected by the invasion stages in the tidal flat. During the initial invasion the environment can offer a large variety of microhabitats for benthos as a result of the low density of S. alterniflora and the environmental characteristics were suitable for gastropod survival (Neira et al. 2007).

However changes occur in the habitat when roots of S. alterniflora harden the sediment and stems and leaves develop above ground after the initial invasion stage; when such changes occur the habitat becomes unsuitable for Bivalvia and Nemertina species (Wang et al. 2010). Therefore habitat changes caused by different S. alterniflora invasion stages (Wang et al. 2006) were a significant influence on C. cingulata spatial distribution.

Although invasion of S. alterniflora changes the density of C. cingulata there was no significant change of the distribution pattern (aggregated) among habitat with different invasion stages in each season (Table II). This phenomenon indicated that the distribution pattern should be determined by the biological characters of species. While the densities changed significantly with the factor of invasion stage and season (Table III Fig. 2). C. cingulata density was lowest during winter (Fig. 2) temperature stress can be a driving force for the seasonal variation of distribution although the effect of migratory birds on C. cingulata density during winter should also be considered (Ge et al. 2011). The western Pacific coast is an important wintering and migration stopover wetland for some bird species (Butler et al. 2001); thus the benthos and birds can be affected each other because they are both involved in a complex food web (Mian 1999).

Of particular note is that in winter the coverage of S. alterniflora was lowest (Table I) the benthos including C. cingulata suffered higher predation risk than other seasons (Shepherd and Lank 2004). The effect of temporal and spatial organization on interspecific associations should be considered when applying to ecosystem management practices of coastal wetlands.

Table III.-###Correlation test of C. cingulate density among seasons (two-tailed and n = 5 in each season).

Spring###Pearson###0.919###0.986###0.914

###correlation###

###P###0.028###0.002###0.030

Summer###Pearson###0.940###0.825

###correlation###

###P###0.018###0.086

Autumn###Pearson###0.873

###correlation###

###P###0.054

ACKNOWLEDGEMENTS

This research was supported by the National Natural Science Foundation of China (31301871 31300443); the Natural Science Foundation of Jiangsu Province (BK20130422); the Natural Science Foundation of the Jiangsu Higher Education Institutions of China (12KJB180016 12KJA180009) and the Opening Foundation of Jiangsu Key Laboratory for Bioresources of Saline Soils (JKLBS2012026).

Statement of conflict of interest There was no conflict of interest from the authors. REFERENCES

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