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

doi:10.21203/rs.3.rs-768072/v1

Download PDF

Research Article

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

https://doi.org/10.21203/rs.3.rs-768072/v1

This work is licensed under a CC BY 4.0 License

You are reading this latest preprint version

Structural complexity of mangrove forests are thought to provide critical habitats for a variety of invertebrates. We studied the influence 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 mudflats. The communities were characterized by the dominance of specific taxa and the comparably low species richness. In total, 18 taxa were identified, including 14 species occurring in the mangrove forest and 16 species in the mudflats. 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 mudflats (54.33±108.69 ind.m^-2). Species such as Haminoea vitrea, Peronia verruculata, Assiminea mesopotamica and Platevindex tigrinus were found to benefit from the presence of pneumatophores, which highlights the importance of local habitat complexity. Gastropod communities varied significantly 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.

Agroecology

Environmental Policy

Arid mangroves

Macrofauna

Diversity

Structural complexity

Persian Gulf

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 km² of mangrove habitats in the Persian Gulf and Gulf of Oman, Iran possesses the highest natural coverage of about 90 km² 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 km². 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 significant 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 significant impacts on energy flow 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.

2.1. Study area and sampling

The study was conducted in Khuran mangrove forest (Fig. 1), where only one tree species exist, i.e. Avicennia marina (Delfan et al., 2021; Shojaei et al., 2019). Tides are semidiurnal with an average height of 2–3 m during spring tides (Sheppard et al., 2010) that usually inundated the mangrove trees to the depth of more than two meters. The mean annual rainfall is about 185 mm (Hajializadeh et al., 2020). Air temperature range from a minimum of 6.4 ºC to 46.6 ºC (Mafi-Gholami et al., 2017). Gastropods were collected in two successive years during February and June 2018 and 2019 from six transects subdivided into two distinct habitats representing the pneumatophore zone and bare mudflats. 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 identification. In the laboratory, species were identified 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).

2.2. 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 fixed factors. Two-way PERMANOVA design with season and habitat as fixed 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).

3.1. Environmental variables

The recorded environmental variables are specified in Table 1. The PCA ordination of the environmental variables revealed clear habitat and seasons clustering (Fig. 2). The first 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 first axis, while temperature was influential along axis 2 (Table 2).

Table 1

Mean (± SD) of environmental variables in Khuran mangrove, Persian Gulf
	Season		Microhabitats
	Winter	Summer	Pneumatophore zone	Muddy bank
PH	7.66 ± 0.11	7.64 ± 0.10	7.60 ± 0.11	7.70 ± 0.09
EC	6.38 ± 2.76	6.29 ± 2.35	7.2 ± 2.51	5.42 ± 2.24
TON	0.04 ± 0.02	0.03 ± 0.02	0.04 ± 0.02	0.03 ± 0.02
TOC	0.59 ± 0.36	0.58 ± 0.30	0.74 ± 0.31	0.41 ± 0.26
Temperature	24.28 ± 1.18	32.17 ± 1.17	28.40 ± 4.27	28.49 ± 4.02
Salinity	31.20 ± 1.03	31.32 ± 1.14	31.30 ± 1.20	31.17 ± 0.96

Table 2

PCA of environmental variables in Khuran mangrove, Persian Gulf
Environmental variables	PC1	PC2	PC3	PC4	PC5
PH	0.506	0.148	0.176	0.361	-0.565
EC	-0.502	0.262	-0.013	-0.167	-0.751
TON	-0.316	-0.275	-0.013	0.88	0.008
TOC	-0.565	-0.167	-0.204	-0.06	0.028
Temperature	-0.193	0.868	0.181	0.226	0.34
Salinity	-0.19	-0.229	0.946	-0.113	0.036

3.2. Gastropods

Results from the gastropod fauna collected within each of the four sampling events (February and June 2018, February and June 2019) indicated a generally consistent pattern among the sampling events. In total, 18 species were found, including 14 species in vegetated habitats and 16 species in un-vegetated habitats. Both habitats had 13 species in common (Table 3). The overall mean of gastropod density was higher at vegetated habitat (86.12 ± 135.21 ind.m^− 2) than un-vegetated mudflats (54.33 ± 108.69 ind.m^− 2). Only four species (Mitrella blanda, M. cartwrighti, Pellamora densilabrum, Pseudominolia sp.) were found in mudflat microhabitats, while two species (Haminoea vitrea, Peronia verruculata) were only found in vegetated microhabitats. The results of two-way ANOVA for the effects of season and habitat on species diversity showed that all diversity indices were significantly higher in summer relative to winter, whereas only Pielou’s evenness index differed significantly between habitats (Table 4 and Fig. 3). In addition, there was no significant interaction between season and habitat. The mean density of gastropods in summer (101.52 ± 144.06 ind.m^− 2) was higher than in winter (44.69 ± 88.48 ind.m^− 2).

Table 3

Taxonomic list and mean density of each taxa in two habitats and seasons in Khuran mangrove, Persian Gulf
			Microhabitats		Season
species	Genus	Family	Pneumatophore zone	Muddy bank	Summer	Winter
Assiminea mesopotamica (Glöer, Naser & Yasser, 2007)	Assiminea	Assimineidae	80	34.96	60.80	60.57
Assiminea sp.	Assiminea	Assimineidae	4.89	7.70	5.48	6.86
Assiminea zubairensis (Glöer & Naser, 2013)	Assiminea	Assimineidae	17.33	8.29	21.03	4
Barleeia sp.	Barleeia	Barleeiidae	2.22	0.59	2.74	0
Cerithidium cerithinum (Philippi, 1849)	Cerithidium	Cerithiidae	0.44	1.18	1.37	0
Cyclostrema ocrinium (Melvill & Standen, 1901)	Cyclostrema	Liotiidae	2.22	1.18	3.20	0
Cyclostrema supremum (Melvill & Standen, 1903)	Cyclostrema	Liotiidae	0.89	2.96	3.20	0
Haminoea vitrea (A. Adams, 1850)	Haminoea	Haminoeidae	6.22	0	6.40	0
Iravadia quadrasi (O. Boettger, 1893)	Iravadia	Iravadiidae	11	12.44	20	1.14
Littoraria intermedia (Philippi, 1846)	Littoraria	Littorinidae	0.44	2.96	2.74	0
Mitrella blanda (G. B. Sowerby I, 1844)	Mitrella	Columbellidae	0	3.55	2.74	0
Mitrella cartwrighti (Melvill, 1897)	Mitrella	Columbellidae	0	1.18	0.91	0
Neverita didyma (Röding, 1798)	Neverita	Naticidae	0.89	2.37	1.82	1.14
Pellamora densilabrum (Melvill, 1912)	Pellamora	Iravadiidae	0	2.37	1.83	0
Peronia verruculata (Cuvier, 1830)	Peronia	Onchidiidae	2.22	0	1.83	0.57
Pirenella cingulata (Gmelin, 1791)	Pirenella	Potamididae	1.08	16.22	6.60	8.78
Platevindex tigrinus (Stoliczka, 1869)	Platevindex	Onchidiidae	15.94	1.77	7.31	13.07
Pseudominolia sp.	Pseudominolia	Trochidae	0	0.59	0.46	0

Table 4

Results of two-way ANOVA of the effects of habitat and season on species diversity indices at Khuran mangrove, Persian Gulf. Statistical significances are indicated in bold.
Margalef richness index					Pielou's evenness
Source	df	Mean Square	F	Sig.	df	Mean Square	F	Sig.
Habitat	1	0.001	0.009	0.927	1	0.119	7.524	0.009
Season	1	0.574	8.035	0.007	1	0.145	9.175	0.004
Habitat * Season	1	0.004	0.054	0.817	1	0.022	1.378	0.247
Error	41	0.071			41	0.016
Shannon-Winer's index					Simpson's diversity index
Source	df	Mean Square	F	Sig.	df	Mean Square	F	Sig.
Habitat	1	0.075	0.523	0.474	1	0.049	2.216	0.144
Season	1	1.509	10.534	0.002	1	0.326	14.593	0.00
Habitat * Season	1	0.041	0.284	0.597	1	0.019	0.851	0.362
Error	41	0.143			41	0.022

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 confirmed 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 significantly 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 significant (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 significant as identified by the marginal test (P < 0.05, Table 7).

Table 5

Results of SIMPER analyses indicating the species contribution to the observed differences in gastropods community structure between seasons and habitats in Khuran mangrove, Persian Gulf
Season (Average dissimilarity = 71.60)
	Winter	Summer
Species	Av.Abund	Av.Abund	Av.Diss	Diss/SD	Contrib%	Cum.%
Assiminea mesopotamica	2.56	2.68	15.57	1.05	21.74	21.74
Pirenella cingulata	1.11	1.6	11.41	0.88	15.94	37.68
Platevindex tigrinus	1.26	1.04	9.91	0.82	13.84	51.51
Assiminea sp.	0.67	0.64	8.15	0.64	11.38	62.89
Assiminea zubairensis	0.55	1.46	8.09	0.82	11.3	74.19
Iravadia quadrasi	0.2	1.12	4.94	0.65	6.9	81.09
Habitats (Average dissimilarity = 75.52)
	Pneumatophore zone	Mudflat
Species	Av.Abund	Av.Abund	Av.Diss	Diss/SD	Contrib%	Cum.%
Assiminea mesopotamica	2.92	2.23	15.57	1.08	20.61	20.61
Platevindex tigrinus	0.64	2.37	14.18	1.03	18.78	39.39
Pirenella cingulata	1.82	0.23	11.07	0.88	14.66	54.05
Assiminea sp.	0.75	0.54	8.14	0.63	10.78	64.82
Assiminea zubairensis	1.2	0.87	7.7	0.8	10.19	75.02
Iravadia quadrasi	0.74	0.68	4.74	0.65	6.28	81.3

Table 6

Results of PERMANOVA for comparing species composition of gastropods in Khuran mangrove, Persian Gulf. Bold values indicate significant level.
Source	df	SS	MS	Pseudo-F	P (perm)
Season	1	3043.6	3043.6	1.132	0.32
Habitat	1	18997	18997	7.0651	0.001
Season × Habitat	1	8.3536	8.3536	0.003	0.983
Res	59	159000	2688.8
Total	62	181000

Table 7

DISTLM marginal tests and the overall best solutions used to identify environmental variables affecting the species composition of gastropods in Khuran mangrove, Persian Gulf. SS (trace) = portion of sum of squares related to the analyzed environmental variable; Pseudo-F = F value by permutation; No. Vars = number of variables; RSS = Residual Sum of Squares. Bold values indicate significant level.
Marginal tests
Variable	SS(trace)	Pseudo-F	P	Prop.
pH	5115.8	1.7711	0.139	2.82E-02
EC	6876.5	2.4046	0.056	3.79E-02
TON	22279	8.5452	0.001	0.12287
TOC	13617	4.953	0.003	7.51E-02
Temperature	3280	1.1238	0.343	1.81E-02
Salinity	2190.3	0.7459	0.589	1.21E-02
Overall best solutions
R²	RSS	No. Vars	Selections
0.21488	1.42E + 05	6	All variables
0.2118	1.43E + 05	5	EC, TON, TOC, Temperature, Salinity
0.20779	1.44E + 05	5	pH, TON, TOC, Temperature, Salinity
0.2064	1.44E + 05	5	pH, EC, TON, TOC, Temperature
0.20458	1.44E + 05	4	TON, TOC, Temperature, Salinity
0.20265	1.45E + 05	4	EC, TON, TOC, Temperature
0.19758	1.45E + 05	4	pH, TON, TOC, Temperature
0.19355	1.46E + 05	3	TON, TOC, Temperature
0.19165	1.47E + 05	5	pH, EC, TON, TOC, Salinity
0.19026	1.47E + 05	5	pH, EC, TON, Temperature, Salinity

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 mudflats. P. tigrinus is very common sea slug in mangrove ecosystem of the Persian Gulf, mostly confined 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 associated fauna (Ashton et al., 2003; Nordhaus et al., 2009). The Khuran mangrove system harbors only one mangrove tree species which provide a homogenous habitat type for different species (Delfan et al., 2021). A low richness of gastropods corresponded with a low diversity of mangrove trees in mangrove system of Qatar (Al-Khayat et al., 2019). Similarity, (Chen et al, (2007) reported that gastropods were low in a rehabilitated mangrove system in Jiulongjiang Estuary, China. Whereas, a high species richness of gastropods was observed in forests with high tree diversity in Indonesia (Nordhaus et al., 2009)

The results of two-way ANOVA for the effects of season and habitat on species diversity showed that all diversity indices significantly differed between seasons, whereas, only Pielou’s evenness index differed significantly between habitats. In addition, there was no significant interaction between season and habitat. Despite this, we observed higher species diversity in pneumatophore zone compared to bare mudflats. The species richness and density of benthic macrofouna has been traditionally attributed to the structural complexity of habitats. The structural complexity of Avicenna aerial roots provides habitat and refuge for resident fauna and the only hard substrates for benthic animal in mangrove habitats (Kamal et al., 2017; Kawaida et al., 2017; Norris et al., 2019). Hard substrates have indirect benefits for primary consumers by providing a settlement for benthic microalgae (Miller et al., 1996; Shahraki et al., 2014). Aerial roots also provides shelter from predators for many invertebrate species and protects resident fauna from wave action and storm surge (Kristensen and Alongi, 2006; Kristensen et al., 2012; Nordhaus et al., 2017). The above-ground structure of mangroves may function as a trap for suspended materials in the ecosystem and thus increasing organic matter input in mangrove habitats (Furukawa et al., 1997; Kamal et al., 2017). The trapping of suspended matters combined with decaying of plant detritus contributes to an abundant food source for gastropods (Nordhaus et al., 2011). In general, the gastropods are detritus feeders and their abundance is subject to the availability of food such as detritus and algae (Akbari et al., 2021; Rahmawati et al., 2015). They prefer habitats protected from currents, waves and direct sunlight (Rahmawati et al., 2015; Zvonareva et al., 2015). The mangrove canopy may also play a significant 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 mudflats. 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).

The results of the current research were in line with results of previous studies which showed that the complexity of aquatic habitats influences 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 mudflats also harbor high value of biodiversity. This lead us to the conclusion that, while conservation efforts have been focused on mangrove forests, adjacent bare mudflats should also be taken into consideration as provides habitat for various mangrove fauna.

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 financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Funding

This research was supported by the Center for International Scientific Studies and Collaboration, Iran (CISSC-grant number: 484).

Ethical approval

No animal testing was performed during this study.

Acknowledgment

We are grateful to students without whom the fieldwork would not have been possible, in particular Nastaran Delfan, Melika Farahani, Rahil Nozarpour, Nazanin Akbari and Khatereh Habibi. The authors are grateful to Dr. Reza Naderloo for his constructive comments. Financial support by the (Grant number: 98018297), is gratefully acknowledged.

Adame, M.F., Reef, R., Santini, N.S., Najera, E., Turschwell, M.P., Hayes, M.A., Masque, P., Lovelock, C.E., 2020. Mangroves in arid regions: Ecology, threats, and opportunities. Estuarine, Coastal and Shelf Science 106796.
Akbari, N., Shojaei, M.G., Weigt, M., 2021. Study on the seasonal changes in food web structure of a mangrove ecosystem using stable isotopes. Master Thesis, Tarbiat Modares University 76.
Al-Khayat, J.A., Abdulla, M.A., Alatalo, J.M., 2019. Diversity of benthic macrofauna and physical parameters of sediments in natural mangroves and in afforested mangroves three decades after compensatory planting. Aquatic Sciences 81, 1–11.
Alfaro, A.C., 2006. Benthic macro-invertebrate community composition within a mangrove/seagrass estuary in northern New Zealand. Estuarine, Coastal and Shelf Science 66, 97–110.
Allison, L.E., 1975. Organic carbon In: Black CA. Methods of soil analysis. American Society of Agronomy, Part 2.
Alongi, D.M., 2008. Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuarine, Coastal and Shelf Science 76, 1–13.
Alongi, D.M., 2002. Present state and future of the world’s mangrove forests. Environmental conservation 29, 331–349.
Ashton, E.C., Macintosh, D.J., Hogarth, P.J., 2003. A baseline study of the diversity and community ecology of crab and molluscan macrofauna in the Sematan mangrove forest, Sarawak, Malaysia. Journal of Tropical Ecology 19, 127–142.
Boström, C., Törnroos, A., Bonsdorff, E., 2010. Invertebrate dispersal and habitat heterogeneity: Expression of biological traits in a seagrass landscape. Journal of Experimental Marine Biology and Ecology 390, 106–117. https://doi.org/10.1016/j.jembe.2010.05.008
Bouillon, S., Connolly, R.M., Lee, S.Y., 2008. Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. Journal of sea research 59, 44–58.
Bouyoucos, G.J., 1962. Hydrometer method improved for making particle size analyses of soils 1. Agronomy journal 54, 464–465.
Bremner, J.M., 1960. Determination of nitrogen in soil by the Kjeldahl method. The Journal of Agricultural Science 55, 11–33.
Chen, G.-C., Ye, Y., Lu, C.-Y., 2007. Changes of macro-benthic faunal community with stand age of rehabilitated Kandelia candel mangrove in Jiulongjiang Estuary, China. Ecological Engineering 31, 215–224.
Clarke, K.R., Gorley, R.N., 2015. Getting started with PRIMER v7. PRIMER-E: Plymouth, Plymouth Marine Laboratory 20.
Clarke, K.R., Gorley, R.N., 2006. Primer. PRIMER-e, Plymouth.
Delfan, N., Ghodrati Shojaei, M., Naderloo, R., 2020. Biodiversity and structure of macrozoobenthos communities in the Hara Biosphere Reserve, Persian Gulf, Iran. Journal of Animal Environment 12, 373–380.
Delfan, N., Shojaei, M.G., Naderloo, R., 2021. Patterns of structural and functional diversity of macrofaunal communities in a subtropical mangrove ecosystem. Estuarine, Coastal and Shelf Science 107288.
Ellis, W.L., Bell, S.S., 2004. Conditional use of mangrove habitats by fishes: depth as a cue to avoid predators. Estuaries 27, 966–976.
Furukawa, K., Wolanski, E., Mueller, H., 1997. Currents and sediment transport in mangrove forests. Estuarine, Coastal and Shelf Science 44, 301–310.
Hajializadeh, P., Safaie, M., Naderloo, R., Shojaei, M.G., Gammal, J., Villnäs, A., Norkko, A., 2020. Species composition and functional traits of macrofauna in different mangrove habitats in the Persian Gulf. Frontiers in Marine Science 7, 1–16.
Hussain, S.A., Badola, R., 2010. Valuing mangrove benefits: contribution of mangrove forests to local livelihoods in Bhitarkanika Conservation Area, East Coast of India. Wetlands Ecology and Management 18, 321–331.
Kamal, S., Warnken, J., Bakhtiyari, M., Lee, S.Y., 2017. Sediment distribution in shallow estuaries at fine scale: in situ evidence of the effects of three-dimensional structural complexity of mangrove pneumatophores. Hydrobiologia 803, 121–132.
Kathiresan, K., Bingham, B.L., 2001. Biology of mangroves and mangrove ecosystems. Advances in marine biology 40, 84–254.
Kawaida, S., Nanjo, K., Kanai, T., Kohno, H., Sano, M., 2017. Microhabitat differences in crab assemblage structures in a subtropical mangrove estuary on Iriomote Island, southern Japan. Fisheries science 83, 1007–1017.
Kiruba-Sankar, R., Krishnan, P., Roy, S.D., Angel, J.R.J., Goutham-Bharathi, M.P., Kumar, K.L., Ragavan, P., Kaliyamoorthy, M., Muruganandam, R., Rajakumari, S., 2018. Structural complexity and tree species composition of mangrove forests of the Andaman Islands, India. Journal of Coastal Conservation 22, 217–234.
Koch, V., Wolff, M., 1996. The mangrove snail Thais kiosquiformis Duclos: A case of life history adaptation to an extreme environment. El caracol de manglar Thais kiosquiformis Duclos: un caso de ciclo vital adaptado a ambientes extremos. Journal of Shellfish Research. 15, 421–432.
Kristensen, E., Alongi, D.M., 2006. Control by fiddler crabs (Uca vocans) and plant roots (Avicennia marina) on carbon, iron, and sulfur biogeochemistry in mangrove sediment. Limnology and Oceanography 51, 1557–1571.
Kristensen, E., Penha-Lopes, G., Delefosse, M., Valdemarsen, T., Quintana, C.O., Banta, G.T., 2012. What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Marine Ecology Progress Series 446, 285–302.
Lee, S.Y., 2008. Mangrove macrobenthos: assemblages, services, and linkages. Journal of Sea Research 59, 16–29.
Macintosh, D.J., Ashton, E.C., 2002. A review of mangrove biodiversity conservation and management. Centre for tropical ecosystems research, University of Aarhus, Denmark.
Mafi-Gholami, D., Mahmoudi, B., Zenner, E.K., 2017. An analysis of the relationship between drought events and mangrove changes along the northern coasts of the Pe rsian Gulf and Oman Sea. Estuarine, Coastal and Shelf Science 199, 141–151.
Miller, D.C., Geider, R.J., MacIntyre, H.L., 1996. Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. II. Role in sediment stability and shallow-water food webs. Estuaries 19, 202–212.
Nagelkerken, I., Blaber, S.J.M., Bouillon, S., Green, P., Haywood, M., Kirton, L.G., Meynecke, J.-O., Pawlik, J., Penrose, H.M., Sasekumar, A., 2008. The habitat function of mangroves for terrestrial and marine fauna: a review. Aquatic botany 89, 155–185.
Nordhaus, I., Hadipudjana, F.A., Janssen, R., Pamungkas, J., 2009. Spatio-temporal variation of macrobenthic communities in the mangrove-fringed Segara Anakan lagoon, Indonesia, affected by anthropogenic activities. Regional Environmental Change 9, 291–313.
Nordhaus, I., Salewski, T., Jennerjahn, T.C., 2017. Interspecific variations in mangrove leaf litter decomposition are related to labile nitrogenous compounds. Estuarine, Coastal and Shelf Science 192, 137–148.
Nordhaus, I., Salewski, T., Jennerjahn, T.C., 2011. Food preferences of mangrove crabs related to leaf nitrogen compounds in the Segara Anakan Lagoon, Java, Indonesia. Journal of Sea Research 65, 414–426.
Nordhaus, I., Wolff, M., Diele, K., 2006. Litter processing and population food intake of the mangrove crab Ucides cordatus in a high intertidal forest in northern Brazil. Estuarine, Coastal and Shelf Science 67, 239–250.
Norris, B.K., Mullarney, J.C., Bryan, K.R., Henderson, S.M., 2019. Turbulence within natural mangrove pneumatophore canopies. Journal of Geophysical Research: Oceans 124, 2263–2288.
Rahmawati, R., Sarong, M.A., Muchlisin, Z.A., Sugianto, S., 2015. Diversity of gastropods in mangrove ecosytem of western coast of Aceh Besar District, Indonesia. Aquaculture, Aquarium, Conservation & Legislation 8, 265–271.
Saenger, P., 2002. Mangrove ecology, silviculture and conservation. Springer Science & Business Media.
Schwamborn, R., Ekau, W., Voss, M., Saint-Paul, U., 2002. How important are mangroves as a carbon source for decapod crustacean larvae in a tropical estuary? Marine Ecology Progress Series 229, 195–205.
Shahraki, M., Fry, B., Krumme, U., Rixen, T., 2014. Microphytobenthos sustain fish food webs in intertidal arid habitats: A comparison between mangrove-lined and un-vegetated creeks in the Persian Gulf. Estuarine, Coastal and Shelf Science 149, 203–212.
Sheppard, C., Al-Husiani, M., Al-Jamali, F., Al-Yamani, F., Baldwin, R., Bishop, J., Benzoni, F., Dutrieux, E., Dulvy, N.K., Durvasula, S.R. V, 2010. The Gulf: a young sea in decline. Marine Pollution Bulletin 60, 13–38.
Sheridan, P., 1997. Benthos of adjacent mangrove, seagrass and non-vegetated habitats in Rookery Bay, Florida, USA. Estuarine, Coastal and Shelf Science 44, 455–469.
Shojaei, M.G., Taheri, A.L.I., Mashhadi Farahani, M., Nastaran, D., Weigt, M., 2019. The role of mangrove primary production in the diet of Thryssa setirostris in Hara Bioshphere Reserve using carbon and nitrogen isotopes. Fisheries Science and Technology 8, 175–181.
Taillardat, P., Friess, D.A., Lupascu, M., 2018. Mangrove blue carbon strategies for climate change mitigation are most effective at the national scale. Biology letters 14, 20180251.
Zvonareva, S., Kantor, Y., Li, X., Britayev, T., 2015. Long-term monitoring of Gastropoda (Mollusca) fauna in planted mangroves in central Vietnam. Zoological studies 54, 1–16.

Download PDF

Reviews received at journal
09 Dec, 2021
Reviewers invited by journal
08 Dec, 2021
Editor invited by journal
13 Aug, 2021
Editor assigned by journal
30 Jul, 2021
First submitted to journal
30 Jul, 2021

You are reading this latest preprint version

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

Status:

Version 1

Abstract

Figures

1. Introduction

2. Materials And Methods

2.1. Study area and sampling

2.2. Statistical analysis

3. Results

3.1. Environmental variables

3.2. Gastropods

4. Discussion

Conclusion

Declarations

Declaration of competing interest

Funding

Ethical approval

Acknowledgment

References

Status:

Version 1