The Effect of Habitat Structural Complexity on Gastropods in Anarid Mangrove Wetland

Structural complexity of mangrove forests are thought to provide critical habitats for a variety of invertebrates. We studied the inuence of mangrove structure and seasonality on the gastropod diversity in the extreme mangrove ecosystem of the Persian Gulf. Sampling was conducted in two successive years (February and June 2018, February and June 2019) at two mangrove habitats i.e., pneumatophore zone and mudats. The communities were characterized by the dominance of specic taxa and the comparably low species richness. In total, 18 taxa were identied, including 14 species occurring in the mangrove forest and 16 species in the mudats. Assimineidae dominated the community in both mangrove habitats. Mean density of gastropods was 1.5-fold higher in the pneumatophore zone (86.12±135.21 ind.m -2 ) than in the mudats (54.33±108.69 ind.m -2 ). Species such as Haminoea vitrea, Peronia verruculata, Assiminea mesopotamica and Platevindex tigrinus were found to benet from the presence of pneumatophores, which highlights the importance of local habitat complexity. Gastropod communities varied signicantly between the habitats, but there was little difference in the community structure between seasons. Distance-based linear models revealed that total organic carbon and total organic nitrogen best explained the variation in gastropods community structure.


Introduction
Mangroves are valuable ecosystems in the intertidal zones of tropical and subtropical coastlines (Adame et al., 2020;Schwamborn et al., 2002). Being among the most productive ecosystems (Alongi, 2002;Bouillon et al., 2008), mangroves are important feeding and nursery grounds for a wide variety of marine species (Nagelkerken et al., 2008). Besides acting as natural barrier by reducing the energy of waves and storm surges (Saenger, 2002), mangroves mitigate climate changes by sequestrating and storing atmosphere carbon dioxide in sediments (Taillardat et al., 2018). In the context of environmental health, mangrove play a crucial role in nutrient recycling and heavy metal remobilization and, therefore, improved water quality (Alongi, 2008;Hussain and Badola, 2010). Out of the total estimated 176 km 2 of mangrove habitats in the Persian Gulf and Gulf of Oman, Iran possesses the highest natural coverage of about 90 km 2 along the southern coasts (Delfan et al., 2021). This represents the northernmost boundary of mangrove distribution in the Indian Ocean. In Iran, the largest mangrove habitat is located in the Hara Biosphere Reserve enclosed between the northern coast of Qeshm Island and the coast of Khamir Port with an area of about 56 km 2 . Only two mangrove species, namely Avicenna marina and Rhizophora mucronata, are present in this region, where the A. marina is the most common species accounting for > 97% of the total tree cover.
Benthic invertebrates shape the structure and functioning of mangrove systems and play signi cant role linking mangrove-derived detritus and higher trophic levels (Lee, 2008;Delfan et al., 2020). Due to their limited mobility, benthic organisms cannot avoid environmental disturbances, which makes them important biotic indicators of coastal system health (Nordhaus et al., 2017). Gastropods are among the predominant groups of macrofauna in mangrove ecosystems (Delfan et al., 2021). They entrap primary production by grazing on fallen leaves and microphytobenthos in mangrove ecosystems (Hajializadeh et al., 2020;Nordhaus et al., 2009). Gastropods can reach a high biomass in mangroves and occupy different levels in the food web and, therefore, have signi cant impacts on energy ow and export of materials to the other ecosystems. In addition, gastropods play critical role in maintaining the productivity of mangroves by cleaning their root systems from encrusting organisms (Koch and Wolff, 1996).
The complexity of mangrove habitats has been shown to have a positive relationship with species diversity (Kamal et al., 2017;Kiruba-Sankar et al., 2018). There is a general consensus that structurally heterogeneous habitats provide a wider range of niches, and different ways of exploiting environmental resources and thus increase species diversity (Kathiresan and Bingham, 2001). Several studies compared macrofauna communities in vegetated and unvegetated habitats and revealed that different microhabitats may contribute differentially to the density, biomass, and diversity (Boström et al., 2010;Macintosh and Ashton, 2002;Sheridan, 1997). However, the majority of reports are based on results of surveys conducted only in tropical systems where productivity is presumably high. To our knowledge, little is known about the effects of vegetation on the macrofauna community composition in arid mangrove systems. The knowledge of macrofauna diversity patterns across different habitat is important for better conservation practices in mangrove habitats (Nordhaus et al., 2006). Here, we examine differences in gastropods community and diversity patterns in mangrove vegetated and unvegetated microhabitats. We hypothesized that vegetated microhabitats would harbor higher diversity of gastropods than unvegetated microhabitats in the Persian Gulf.

Study area and sampling
The study was conducted in Khuran mangrove forest (Fig. 1), where only one tree species exist, i. the pneumatophore zone and bare mud ats. Three quadrats (25×25 cm) were placed on the substrates from which organisms were hand-picked. Only live-collected specimens were taken into account, since empty shells can obscure the real diversity of gastropods. Gastropods were preserved in 70% ethanol for later identi cation.
In the laboratory, species were identi ed to the lowest possible taxonomic level and the number of individuals were counted. Four environmental parameters were measured at each site including pH, salinity, temperature, and electric conductivity (EC) using portable device. Sediment samples were also taken for determination of sediment geochemistry, using sampling corer of 5 cm diameter and 5 cm depth. Samples were placed in plastic bags, labeled, and were kept at 4 ºC until they were oven-dried at 60 ºC. Total organic carbon (TOC) and total organic nitrogen (TON) were determined using Walkley-Black (Allison, 1975) and Kjeldahl methods (Bremner, 1960), respectivly. In addition, the percentage of silt, sand and clay were determined using hydrometry methods (Bouyoucos, 1962). An environmental data matrix transformed (log x + 1) and normalized prior to analyses (Clarke and Gorley, 2006).

Statistical analysis
For species diversity indices, i.e., Margalef's richness, Shannon-Wiener index (H′), Simpson, and Pielou's evenness index (J′), were calculated using DIVERSE analysis (Clarke and Gorley, 2015). Two-way ANOVA was used to analyze the effect of habitats and seasons on species diversity indices. Taxonomic similarity between samples was calculated based on Bray-Curtis distance, whereas the similarity matrix of environmental variables were calculated using normalized Euclidean distance. Non-metric multidimensional scaling (nMDS) was used to visualize the possible similarity of gastropods composition between habitats and seasons. Similarity percentage analysis (SIMPER) analysis was used to identify the species that contributed most to differences between xed factors. Two-way PERMANOVA design with season and habitat as xed factors was used to determine the main effects of habitats and seasons on species composition. Spearman correlation was used to determine a collinearity among environmental variables. As none was collinear, all variables were tested. The univariate analysis was performed using SPSS (Version 16.0, SPSS Inc., Chicago, IL) and multivariate analysis was performed using Primer + PERMANOVA software package (PRIMER-E Ltd).

Environmental variables
The recorded environmental variables are speci ed in Table 1. The PCA ordination of the environmental variables revealed clear habitat and seasons clustering (Fig. 2). The rst two principal components explained 59.8% (PCA1 = 42.6%, PCA2 = 17.2%) of the variability in environmental data over the seasons and microhabitats. TOC, pH and EC were the major determinants of differences between seasons along the rst axis, while temperature was in uential along axis 2 ( Table 2).   The MDS plots for gastropod communities revealed a clear separation between habitats (Fig. 4a), whereas no clear separation was found between summers and winter (Fig. 4b). The ANOSIM tests con rmed the differences on the structure of gastropods communities between habitats (Global R = 0.17, p = 0.001, number of permutations = 999).
A SIMPER analysis was used to identify the role of individual species in contribution to the dissimilarity between microhabitats and seasons ( Table 5). The average dissimilarity was 71.60% between seasons, mainly due to the presence of Assiminea mesopotamica, Pirenielia cingulate and Platevindex tigrinus accounting for 51.51% of the dissimilarity between seasons ( Table 5). The average dissimilarities between habitats was 75.52% which was mostly explained by A. mesopotamica, P. tigrinus and P. cingulate accounting for 54.05% of dissimilarity between microhabitats (Table 5). Two-way PERMANOVA analysis for effects of habitat and season showed that only habitat signi cantly affected the species composition (F = 7.06, P = 0.001), whereas the effects of season as well as the interaction between habitat and season were not signi cant (Table 6). According to DISTLM analysis, the best model was achieved by a combination all environmental variables which accounted for 21.49% of the variability of the data (Table 7). For species composition only TON, TOC were signi cant as identi ed by the marginal test (P < 0.05, Table 7).

Discussion
The results of the current study revealed a distinct community composition of gastropods in different habitats of Khuran mangrove ecosystem in the Persian Gulf. A. mesopotamica and P. tigrinus were the dominant species in pneumatophore zone which highlighted their importance in shaping the gastropod community structure in mangrove ecosystem. In contrast, Pirenella cingulate and Littoraria intermedia were the dominant species in mud ats. P. tigrinus is very common sea slug in mangrove ecosystem of the Persian Gulf, mostly con ned within the A. marina fringe (Hajializadeh et al., 2020). As a dominant grazer and representing important component in the food web dynamics of this mangroves, P. tigrinus actively forages for microbial mats and mangrove leaf litter at low tide (Akbari et al., 2021). It avoids being covered by water at high tide by climbing various parts of mangrove trees (personal obs.). Adult snails are preyed upon by gray heron Ardea cinerea and western reef heron Egretta gularisand the juveniles may be preyed on by crabs (personal obs.).
Overall, species richness of gastropods in Khuran mangrove system was low despite being a relatively undisturbed habitat. For example, around 50 species were found in Malay peninsula (Macintosh and Ashton, 2002), 30 species in the west coast of Thailand (Macintosh et al., 2002), and 41 species in the Segara Anakan lagoon, Indonesia (Nordhaus et al., 2009). In general, species richness of mangrove gastropods parallel to that of mangrove trees, as higher mangrove species richness provide different habitat types and food source for . The mangrove canopy may also play a signi cant role in shaping the gastropod community in the pneumatophore zone (Ellis and Bell, 2004). In arid mangrove ecosystem of the Persian Gulf, shade provides refuge from desiccation and heat stress as these areas have lower temperatures than bare mud ats. Shade reduces the visibility of gastropods, making them less vulnerable to some predators. In line with the results of the current study, Sheridan (1997) reported a higher density of macrofouna in mangrove habitats compared to bare habitats. In contrast, Alfaro (2006) found that mangrove habitat had the lowest diversity among the six marine habitats in New Zealand. The observed contradiction is probably due to different sampling periods and methodologies (Nordhaus et al., 2009;Sheridan, 1997).

Conclusion
The results of the current research were in line with results of previous studies which showed that the complexity of aquatic habitats in uences the density of gastropods. The characterization of gastropods communities within mangrove stands and adjacent mudfalts at Khuran strait, northern Persian Gulf, indicated that while mangroves yield a higher density and diversity of gastropods, adjacent mud ats also harbor high value of biodiversity. This lead us to the conclusion that, while conservation efforts have been focused on mangrove forests, adjacent bare mud ats should also be taken into consideration as provides habitat for various mangrove fauna.

Declarations
Aauthorship contribution HE and MGS designed the study, collected the data. HE, MGS, and JS, analyzed the data and wrote a draft of the manuscript. All authors contributed to the revision of the work.

Declaration of competing interest
The authors declare that they have no known competing nancial interests or personal relationships that could have appeared to in uence the work reported in this paper.

Funding
This research was supported by the Center for International Scienti c Studies and Collaboration, Iran (CISSCgrant number: 484).

Ethical approval
No animal testing was performed during this study. Comparison of diversity indices between seasons (winter and summer) and habitats in Khuran mangrove, Persian Gulf, between (a) habitats (P = pneumatophore zone and M = mud ats) and (b) seasons (W = winter and S = summer)