Benthic macrofaunal dispersion within different mangrove habitats in Hara Biosphere Reserve, Persian Gulf

Abstract

The community composition of benthic macrofauna and relationships between physiochemical parameters of the water and sediment texture were assessed in Hara Biosphere Reserve, Northern Persian Gulf. The spatial distribution and diversity of macrobenthos were sampled within three distinctive mangrove zones (deltaic, island and coastal) during two sampling seasons between August 2014 and January 2015. A total of nine transects perpendicular to the coastline were selected to cover over the entire study area. The counts of all macrofauna were recorded from each zone and station with three replicate sediment samples. The snails, Cerithidea cingulata and Asseminea sp., were observed throughout three mangrove zones, but their abundance varied among habitats. The bivalve Dosinia ceylonica found to be more abundant in delta, whereas burrowing crabs Ocypode and Uca were dominate in coastal zone. Terebralia palustris and amphipods were recorded frequently in island zone. The nonmetric multidimensional scaling ordinations and a three-way factor PERMANOVA indicated that macro-invertebrate species composition significantly differed among different mangrove zones. The results also showed the seasonal variations. The findings of diversity indices illustrated that deltaic zone had the highest abundance and diversity, while the coastal zone showed the lowest values among the three zones. Taken together, the observations demonstrated that the different hydrological conditions, temperature, salinity and sediment texture were the main factors determining dispersion of benthic faunal assemblages among different mangrove habitats at Hara Biosphere Reserve. There is a need to consider such variables in ecological studies to understand differences of macrofaunal diversities in these complex habitats.

Full text

1 23
International Journal of
Environmental Science and
Technology
ISSN 1735-1472
Int. J. Environ. Sci. Technol.
DOI 10.1007/s13762-019-02469-2
Benthic macrofaunal dispersion within
different mangrove habitats in Hara
Biosphere Reserve, Persian Gulf
F.Vahidi, S.M.R.Fatemi, A.Danehkar,
A.Mashinchian & R.Musavi Nadushan

1 23
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Vol.:(0123456789)
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International Journal of Environmental Science and Technology
https://doi.org/10.1007/s13762-019-02469-2
ORIGINAL PAPER
Benthic macrofaunal dispersion withindierent mangrove habitats
inHara Biosphere Reserve, Persian Gulf
F.Vahidi1· S.M.R.Fatemi1· A.Danehkar2· A.Mashinchian1· R.MusaviNadushan1
Received: 13 September 2017 / Revised: 9 June 2019 / Accepted: 3 July 2019
© Islamic Azad University (IAU) 2019
Abstract
The community composition of benthic macrofauna and relationships between physiochemical parameters of the water and
sediment texture were assessed in Hara Biosphere Reserve, Northern Persian Gulf. The spatial distribution and diversity
of macrobenthos were sampled within three distinctive mangrove zones (deltaic, island and coastal) during two sampling
seasons between August 2014 and January 2015. A total of nine transects perpendicular to the coastline were selected to
cover over the entire study area. The counts of all macrofauna were recorded from each zone and station with three replicate
sediment samples. The snails, Cerithidea cingulata and Asseminea sp., were observed throughout three mangrove zones, but
their abundance varied among habitats. The bivalve Dosinia ceylonica found to be more abundant in delta, whereas burrow-
ing crabs Ocypode and Uca were dominate in coastal zone. Terebralia palustris and amphipods were recorded frequently
in island zone. The nonmetric multidimensional scaling ordinations and a three-way factor PERMANOVA indicated that
macro-invertebrate species composition significantly differed among different mangrove zones. The results also showed the
seasonal variations. The findings of diversity indices illustrated that deltaic zone had the highest abundance and diversity,
while the coastal zone showed the lowest values among the three zones. Taken together, the observations demonstrated that
the different hydrological conditions, temperature, salinity and sediment texture were the main factors determining dispersion
of benthic faunal assemblages among different mangrove habitats at Hara Biosphere Reserve. There is a need to consider
such variables in ecological studies to understand differences of macrofaunal diversities in these complex habitats.
Keywords Biodiversity· Macro-invertebrates· Mangrove ecosystem· Seasonal variation
Introduction
Mangroves are intertidal biogeochemically active habi-
tats occurring at the interface between land and sea in
tropical and subtropical latitudes, and they also exist
under conditions of high salinity, extreme tides, strong
winds, high temperature and muddy anaerobic soils
(Kathiresan and Bingham 2001; Nagelkerken etal.
2008). They are habitats for a wide variety of organisms;
some of them occurring in high densities provide food,
breeding grounds and nursery sites for a large number of
commercially valuable finfish and shellfishes (Carugati
etal. 2018).
The mangrove forests consist of many different vegetation
structures. They also sustain a diverse and distinct assem-
blage of benthic organisms, which are various in size from
the minute bacteria and protozoans to larger (0.5 < mm size)
invertebrates known as macrobenthos (Roberts 2006; Zaka-
ria and Rajpar 2015). Gastropods, polychaetes and crusta-
ceans as mangrove inhabitants are found to be the major
invertebrate groups (Thilagavathi etal. 2013; Kabir etal.
2014). These organisms could play an important ecological
role in the structure and function of marine coastal ecosys-
tems (Saulnier etal. 2018).
Benthic macrofaunal communities may vary from habi-
tat to habitat within the same mangrove forest (Tang and
Yu 2007; Dissanayake and Chandrasekara 2014). They
often exhibit a specific horizontal and vertical zonation
pattern (Sivasothi 2000). Distribution of macrofaunal
Editorial responsibility: S. R. Sabbagh-Yazdi.
* S. M. R. Fatemi
reza_fatemi@hotmail.com
1 Department ofMarine Biology, Science andResearch
Branch, Islamic Azad University, Tehran, Iran
2 Faculty ofNatural Resource, University ofTehran, Karaj,
Iran
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International Journal of Environmental Science and Technology
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assemblage is influenced by local environmental condi-
tions such as hydrological characteristics, physicochemi-
cal factors (pH, temperature, salinity), tidal patterns,
availability of organic matter, sediment texture, predation,
competition and human activities (Lee 2008; Sihombing
etal. 2017). Hence, the most successful benthic species in
mangrove habitats are those organisms that easily adapt to
the prevailing environmental properties of these ecosys-
tems (Dissanayake and Chandrasekara 2014).
Several studies have revealed the biological produc-
tivity and biodiversity of mangrove habitats in tropical
and subtropical regions. Pawar (2015) indicated that the
mangrove ecosystem of Uran is heavily contaminated
by the sewage, and macrobenthic fauna is threatened by
the anthropogenic stress. Thivakaran and Sawale (2016)
in a study found that vegetation structure composed of
single species and abiotic factors were assigned for the
uniform macrofaunal community composition in the two
mangrove formations. Bernardino etal. (2017) evaluated
the changes in benthic macrofaunal communities and food
webs in a case of mangrove removal and natural sites in a
tropical estuary. They found that the benthic assemblage
composition significantly differed in the impacted site
being strongly related to sedimentary changes. Despite
the wealth of knowledge on the importance of mangrove
forests at the global scale (Netto and Gallucci 2003; Sara-
vnakumar etal. 2007), there is insufficient information
focusing on the effects of mangrove zonation on benthic
macrofaunal assemblages. Nevertheless, some researchers
have determined differences in macrobenthic community
composition in relation to the function of mangrove dis-
tribution. For example, Dissanayake and Chandrasekara
(2014) in a study revealed that the physicochemical fac-
tors varied in the sediment among the three mangrove
habitats, and the diversity of infaunal community was
a function of the mangrove zonation. Samidurai etal.
(2012) reported that the diversity of macrobenthic species
in riverine mangrove is comparatively higher than that of
the developing and island mangroves due to the hydro-
graphic, nutrients and sediment texture. Alfaro (2006)
also found distinctive faunal assemblages within different
habitats such as mangrove stands, pneumatophore zones
and channels, as the lowest number of macrobenthos taxa
was found in mangrove areas. In Iran, some studies have
been performed in the mangrove environments to inves-
tigate the benthic community composition, though they
were not restricted to this study area (Ghasemi etal. 2011;
Safahieh etal. 2012; Aghajanpour etal. 2015; Kamalifar
etal. 2016). Aghajanpour etal. (2015) introduced mobile
gastropods as the dominant macro-invertebrate associated
with the tidal mangrove trees. Furthermore, comparative
studies carried out between two mangrove stands of Iran
have revealed differences in benthic (only gastropods)
abundance and diversity associated with different kinds of
mangrove (Ghasemi etal. 2011). Kamalifar etal. (2016)
reported that the macrobenthic community structure in
Bidkhun mangrove swamp was significantly influenced
by the environmental variables such as sediment texture,
TOC and seasonal temperature.
Although these studies provided the initial evidence
that different habitats may contribute differentially to
the biodiversity of Iranian mangroves, to date there has
been no comprehensive research to assess the ecological
value of these ecosystems. Baseline information, monitor-
ing programs and experimental trials are required before
ecological assessments to provide adequate ecological
value from the Iranian mangroves. The present research
was designed to investigate and compare the key benthic
macrofaunal species within distinctive mangrove habitats
in (island, coastal and deltaic mangrove) Hara Biosphere
Reserve. For this purpose, the study was carried out in
the coldest (January 2015) and the warmest (August
2014) months of the year. This study is considered as the
first step for evaluating the relative importance of habi-
tats with different structures and complexities in Iranian
mangrove ecosystems.
Materials andmethods
The study site
The present study was performed at the Hara Bio-
sphere Reserve with an area of 85,686ha (36°40′ to
37° and 55°21′ to 55°52′E) (Fig.1). It is located in the
south of Iran in the Straits of Khuran between Qeshm
Island and the Persian Gulf. Ramsar convention has
introduced this region as an international wetland and
named it Khouran Straits. It hosts the largest mangrove
species of Avicennia marina along the Persian Gulf
shoreline, therefore representing a center of biodiver-
sity in Iran. Mangroves are distributed throughout the
study area in a variety of habitats. Due to the hydro-
logical conditions, there is a distinct mangrove zona-
tion pattern (i.e., deltaic mangrove, island mangrove
and costal mangrove) in the Hara Biosphere Reserve
(Danehkar 2007). Deltaic mangrove zone (2163ha) is
connected to the open sea of the Persian Gulf from
one side and Mehran River delta from another side.
It is a dynamic area of mixed-water flow and salinity.
The island mangrove zone is connected to the Persian
Gulf from all sides. It has the largest spatial spread-
ing in the study area (3425ha). The coastal mangrove
zone (2035ha) is connected to the Persian Gulf from
one direction and a land locked by the coast. The tidal
regime of research area is semidiurnal, with minimum
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International Journal of Environmental Science and Technology
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and maximum tidal ranges of 0.3m and 4.6m, respec-
tively. In the study area, mangroves are classified into
dense (> 75% cover), moderately dense (25–75% cover)
and sparse (< 25%) based on the canopy cover percent-
age (Danehkar 2007). The variety of mangrove zones
and relatively high diversity of species have made this
region an ideal site to study macrobenthic community
composition across different habitat gradients.
Sampling program
Because of two natural seasons (cold season and warm
season) in south of Iran (Aghajanpour etal. 2015), the
sampling was performed at the peak of each natural
season (as defined by the climatological parameters,
e.g., on the coldest (January 2015) and the warmest
(August 2014) months of the year) during high tide at
the sampling locations throughout the study period.
Within each mangrove zone (deltaic, island and
coastal), three transect lines were placed perpendicular
to the coastline based on the canopy cover percentage
(dense, moderate, sparse). Then, three stations were
determined in each transect. The geographic positions
of each station and sampling time were recorded by
handheld GPS.
Environmental sampling
Ekman Bottom Grab (225cm2) was used to collect sedi-
ment samples for sediment grain size and infaunal analy-
sis. Three replicate sediment samples were taken from
each zone and station during each sampling event for
grain size analysis and determining total organic mate-
rial. The particle of the sediment was characterized by
mechanical sieving or by a Horiba LA-950 laser particle
size analyzer (LA-950, Horiba). Analysis of total organic
matter (TOM) was conducted by burning the sediment
1
2
3
A
B
C
C- 3
A-1
A-2
B-3
B-1
B-2 C-2
A-3
C- 1
Fig. 1 Map of the sampling sites at Hara Biosphere Reserve, northern Persian Gulf; transect lines are demonstrated within three zones across
different habitats
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in a furnace at 450°C for 5h (Neria and Hopner 1994).
Measurements of water temperature, salinity, dissolved
oxygen and pH were recorded at each of the 27 sampling
stations to identity relative differences among locations
during each sampling event.
Biological sampling
Benthic fauna were sampled using Ekman Bottom Grab
(225cm2) in August 2014 and January 2015. Three replicate
sediments were collected for macrofauna within each zone
at each station. All samples were sieved through a 0.5mm
mesh. Counts of all macrofauna were recorded, followed
by species identification to the lowest possible taxonomic
level using available reference texts. In most cases, spe-
cies was considered as the lowest taxonomic level (Smythe
1982; Jones 1986; Bosch etal. 1995; Carpenter etal. 1997;
McLaughlin 2003; Poore 2004; Kazmi and Siddiqui 2006).
Identifications were confirmed by the taxonomists at Uni-
versity of Tehran.
Data analysis
Macrofauna taxa collected from the beds were identified
and listed. Macrofaunal community was assessed in terms
of the Shannon–Wiener diversity (H), Pielou’s species
evenness (J) and Margalef species richness (D) sepa-
rately for each mangrove zone. The relationship between
environmental variables (i.e., temperature, salinity, pH,
dissolved oxygen and sediment texture) and macrofaunal
community indices was assessed using Pearson correla-
tion coefficients.
The variations in environmental variables between
the three mangrove zones were analyzed by one-way
analysis of variance (ANOVA). Multiple comparisons
were conducted using Tukey’s test. A three-factor (fac-
tor 1 = season, fixed, two levels: cold and warm, fac-
tor 2 = zone, fixed, three levels: deltaic, island and cos-
tal mangrove, factor 3 = canopy cover percentage, fixed,
three levels: dense, moderately and sparse) permutational
MANOVA (PERMANOVA) (Anderson 2001), with a type
I model, was used to analyze the data. Sample abundance
data were fourth-root transformed to meet the homosce-
dasticity assumption. Significant differences were tested
at p = 0.05 using 9999 permutations with Bray–Curtis
similarity (Dorman etal. 2012). In the case of significant
differences for the PERMANOVA main test, pairwise test
was used to compare the significance levels of the factors.
Principal components analysis (PCA) was utilized to detect
the relationships between the variations in spatial patterns
of the most abundant taxa and environmental factors (Leps
and Smilauer 2003). Nonmetric multidimensional scaling
(nMDS) was computed based on the Bray–Curtis similarity
matrix using fourth-root-transformed abundances of mac-
rofauna to detect the groupings of mangrove zones (Clarke
and Warwick 2001). SPSS (Statistical package v.16.0),
software of PRIMER (Plymouth Routines In Multivariate
Ecological Research v.6.0) and CANOCO program (v.5.0)
were used for statistical analyses.
Results anddiscussion
Environmental parameters
In the Hara Biosphere Reserve, spatial variations of
physicochemical parameters were found to be similar
throughout the study period, indicating the well-mixed
nature of this ecosystem. Water temperature ranged
Table 1 Summary of the physicochemical parameters of the water across the three mangrove zones (deltaic, island and coastal) in the Hara Bio-
sphere Reserve
Values are mean ± SE, range in parenthesis. Different lower case letters in a row denote significant differences (p < 0.05) indicated by Tukey’s
pairwise significant difference test
*Significantly calculated p value detected by ANOVA
Physicochemical parameters Deltaic zone Island zone Coastal zone
Cold War m Cold Warm Cold Wa rm
Temperature (°C) 22.81 ± 0.28 35.54 ± 1.11 22.75 ± 0.34 36.18 ± 1.26 22.46 ± 0.53 34.32 ± 0.87
29.17 ± 6.59 29.47 ± 6.96 28.34 ± 5.57
Dissolved oxygen (mg/l) 8.51 ± 0.09 6.56 ± 0.37 8.50 ± 0.23 6.87 ± 0.43 8.76 ± 0. 29 5.85 ± 0.41
7.53 ± 1.03 7.68 ± 0.90 7.31 ± 1.54
pH* 8.58 ± 0.06 8.47 ± 0.04 8.50 ± 0.11 8.48 ± 0.07 8.47 ± 0. 11 8.38 ± 0.04
8.53 ± 0.07a8.49 ± 0.08ab 8.43 ± 0.10b
Salinity (ppt) 36.33 ± 1.80 44.66 ± 1.11 35.33 ± 1.08 44.44 ± 1.42 36.22 ± 0.83 42.55 ± 2.35
40.5 ± 4.52 39.88 ± 4.83 39.88 ± 3.23
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from 22.3 to 24.1°C in winter and from 32 to 37.8°C
in summer. Salinity and dissolved oxygen measure-
ments were recorded during high tide at the sampling
stations, and they were reported to be ranged from 34
to 47ppt and 5 to 9.2ppm, respectively. The ranges of
these factors indicated the strong influence of tidal cur-
rents and saltwater inputs in this intertidal mangrove
forest. The pH value was found to be ranged from 8.2
to 8.7 during the study (Table1). The results of the
one-way ANOVA and variations in the physicochemical
factors across the three mangrove zones are presented
in Table1. A significant or nonsignificant difference
was found in almost all these factors between the three
mangrove zones.
The highest organic content was in the coastal zone,
while the deltaic zone had the minimum organic content.
In terms of the sediment texture, percentages of sand (%)
and silt–clay (%) were reported to be ranged as 2.89–70.68
and 29.32–97.11, respectively (Table2). Silt–clay was most
abundant in the coastal zone, while sand was dominant in
the deltaic zone. The results of one-way ANOVA showed
nonsignificant differences for all sediment characteristics
among stations and zones (p > 0/05).
Species composition ofmacrofauna
A large number of studies have highlighted the biodiversity
and ecological importance of mangrove habitats through-
out the world. On the other hand, few studies have been
conducted to assess the effects of mangrove zonation on
the benthic macrofaunal assemblages. As the Iranian Hara
Biosphere Reserve has not been assessed so far, it was pro-
posed to study the biodiversity conservation of the mangrove
forests.
The results obtained from the assessment of benthic
invertebrates samples indicated a generally seasonal and
spatial pattern among the sampling events. This inter-
tidal fauna seems to have been adapted to the harsh envi-
ronmental conditions such as high temperature, exces-
sive evaporation and a trend of fluctuations in salinity
and tidal ranges. These environmental parameters exert
a strong effect on faunal communities to tolerate the
situation.
In the present study, 51 macrobenthic faunal species were
represented by five diverse groups, of which gastropods,
bivalves, crustacea, polychaetes and oligochaetes were the
most important groups (Table3).
Gastropods were dominant in the macrobenthic fauna
(24 species) and were accounted for up to 38.09% of the
population. Crustaceans consist of seven species account-
ing for 24.41%, and bivalves with nine species constituted
24.53%. Polychaetes consist of eight species and cover
10.62% of the population, while oligochaetes accounted
for 2.35% of the total macrobenthic fauna population
(Fig.2). Figure2a–d shows that the most variation in
the percentage composition of macrofauna was observed
for bivalvia and crustacean among three mangrove zones.
The macrobenthos was dominated by the bivalve, Dosinia
ceylonica, and the ghost crab, Ocypode sp, strongly
peaking during the cold season. Mud whelk, Cerithidea
cingulata, and the snail, Asseminea sp, appeared to be
associated with the superficial mudflat sediments during
the warm season. Other Iranian studies have reported the
presence of snails, Cerithidea cingulata, and Hydrobia sp
(abundant species), the bivalve, Paphiagalus, and the mud
crab, Macrophthalmus pectinipes, within mangrove habi-
tats (Ghasemi etal. 2011; Safahieh etal. 2012; Aghajan-
pour etal. 2015).
Distribution patterns ofbenthic macrofauna
indierent mangrove zones
The snails, Cerithidea cingulata and Asseminea sp., were
present throughout all the study zones and stations, but
their abundance varied across different habitats (delta:
135.5 ± 177.6 and 132.3 ± 193.7 ind/m−2, respectively;
island: 60 ± 93.5 and 17 ± 55.8 ind/m−2, respectively; and
coastal: 41 ± 85.5 and 24 ± 45.9 ind/m−2, respectively).
White clam (Dosinia ceylonica) was mainly found in the
delta (241.8 ± 360.3 ind/m−2), while burrowing crabs
(i.e., Ocypode and Uca) were observed with higher abun-
dances (±) in the coastal (47 ± 43.7 and 24 ± 20.1ind/m−2,
Table 2 Mean (± SE) values for sediment characteristics (grain size and organic content) within three mangrove zones (deltaic, island and
coastal) in the Hara Biosphere Reserve
Sediment texture Deltaic zone Island zone Coastal zone
Cold War m Cold Warm Cold Wa rm
Total organic matter (%) 3.92 ± 1.18 4.00 ± 0.70 4.12 ± 1.58 3.97 ± 1.36 5.76 ± 2.29 4.51 ± 2.05
Silt–clay (%) 55.99 ± 16.34 83.32 ± 17.95 60.89 ± 20.67 83.16 ± 18.27 69.86 ± 14.43 85.52 ± 6.75
Sand (%) 44.00 ± 16.34 16.67 ± 17.95 39.10 ± 20.67 16.83 ± 18.27 30.13 ± 14.43 14.47 ± 6.75
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Table 3 Species recorded during the study period
Faunal group Order Family Genus Species Deltaic Island Coastal
Bivalvia Myoida Corbulidae Corbula Corbula modesta 31 10 0
Arcoida Arcidae Barbatia Barbatia sp 29 5 3
Ostreoida Ostreoidae Saccostrea Saccostrea cucullata 18 11 8
Veneroida Donacidae Donax Donax scalpellum 6 0 1
Tellinidae Eurytellina Eurytellina natalensis 9 4 0
Tellinidae Serratina Serratina capsoides 2 0 0
Trapeziidae Trapezium Trapezium sublaevigatum 1 0 0
Veneridae Phapia Phapia cor 10 8 2
Dosinia Dosinia ceylonica 241 11 0
Gastropoda Patellogastropoda Liotiidae Cyclostrema Cyclostrema ocrinium 3 0 0
Cyclostrema supremum 2 0 0
Neogastropoda Columbellidae Mitrella Mitrella blanda 3 0 0
Mitrella misera 8 2 0
Anachis Anachis misera 8 1 0
Terebridae Terebra Terebra sp. 1 1 0
Littorinimorpha Assimineidae Asseminea Asseminea bedomeana 2 1 4
Asseminea sp. 132 17 24
Stenothyra Stenothyra Stenothyra arabica 2 0 3
Iravadiidae Lucidinella Lucidinella densilabrum 5 2 0
Iravadia Iravadia quadrasi 5 0 2
Littorinidae Littoraria Littoraria intermedia 11 5 11
Caenogastropoda Potamididae Telescopium Telescopium telescopium 2 1 0
Cerithidea Cerithidea cingulata 136 60 41
Terebalia Terebalia palustris 41 64 17
Cerithiidae Cerithium Cerithium cerithium 1 0 0
Epitoniidae Epitonium Epitonium pallasii 1 1 0
Vetigastropoda Calliostomatidae Calliostoma Calliostoma sp. 0 1 0
Trochidae Umbonium Umbonium vestiarium 5 1 0
Microascales Halosphaeriaceae Turitella Turitella sp. 10 1 0
Panpulmonata Pyramidellidae Turbonilla Turbonilla linjaica 2 0 0
Pulmonata Amphibolidae Salinator Salinator fragilis 2 0 0
Systellommatophora Onchidiidae Onchidium tigrinum 0 5 0
Babyionia spirata 2 1 2
Crustacea Sessilia Balanidae Balanus Balanus amphitrite 11 22 16
Decapoda Macrophthalmidae Macrophthalmus Macrophthalmus sulcatus 8 7 8
Ocypodidae Uca Uca sp 16 37 24
Ocypode Ocypode sp. 59 66 47
Varunidae Metaplax Metaplax indica 2 1 1
Amphipoda 28 63 4
Polychaeta Orbiniida Orbiniidae Scoloplos Scoloplos sp. 11 32 15
Magelonidae Magelona Magelona sp. 12 0 0
Phyllodocida Nereididae Lycastopsis sp. 4 3 5
Neanthes sp. 6 0 9
Nephtyidae Nephtys sp. 14 40 8
Spionida Spionidae Prionospio Prionospio sp. 4 1 1
Terebellida Cirratulidae Cirriformia Cirriformia sp. 7 0 1
Eunicida Lumbrinereidae Lumbrineris. Lumbrineris sp. 0 6 3
Oligochaeta Unknown oligochaetes 10 10 20
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respectively) zone. Furthermore, the mud whelk Terebralia
palustris (64 ± 173.4) and benthic crustaceans including
amphipods and some crabs were most abundant (±) in the
island zone.
A three-way factor PERMANOVA was done to investi-
gate the effects of season, zone and canopy cover percent-
age on the macrofaunal assemblage structure. The results
of PERMANOVA showed significant effects of season
and zone on the assemblage composition (p < 0.05),
but there was no significant effect for the canopy cover
percentage. There was no also significant interaction
between the three factors. However, follow-up pairwise
tests between zones revealed significant differences
between the delta and two other zones (Table4, Fig.3).
Accordingly, the macrofaunal communities of three
mangrove zones exhibited distinct variations. These dis-
tinct differences suggested that while some species were
found throughout all zones, most species tended to show
24.53%
38.09%
24.41%
10.62% 2.35%
A Overall species composition
Bivalvia
Gastropoda
Crustacea
Polychaeta
oligochaeta
9.84%
32.53%
39.36%
16.27% 2.01%
B Island
Bivalvia
Gastropoda
Crustacea
Polychaeta
oligochaeta
38.01%
41.47%
13.17%
6.26% 1.08%
C Deltaic
Bivalvia
Gastropoda
Crustacea
Polychaeta
oligochaeta
6.07%
36.79%
35.00%
15.00%
7.14%
D Coastal
Bivalvia
Gastropoda
Crustacea
Polychaeta
oligochaeta
Fig. 2 Percentage composition of macrobenthos in different mangrove zones
Table 4 Results of PERMANOVA and pairwise comparisons between the seasons, zones and canopy cover percentage
*Significance shown at the 0.05 level
Factor df MS Pseudo-F P (perm)
Season 1 3594 8.65 0.0001*
Zone 2 1155 2.78 0.02*
Percent canopy cover 2 372 0.89 0.49
t value P (perm)
Pairwise comparisons (season and zone)
Season
Cold. Warm 3.005 0.0001*
Zone
Delta. Island 1.92 0.02*
Delta. Coastal 1.93 0.02*
Coastal. Island 1.20 0.27
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International Journal of Environmental Science and Technology
1 3
a special dispersal strategy. For example, in the deltaic
zone, the macrobenthic community was mainly domi-
nated by the suspension feeders such as venerid bivalve
Dosinia ceylonica, positively correlated with suspended
materials. Specifically, the frequency of inundation and
stronger tidal current have provided the food (suspended
particle) for suspension feeders (bivalves), leading to the
increase in their abundance in the deltaic zone. Gills etal.
(2012) also found that Dosinia ceylonica as a special-
ist suspension feeder has a preference mangrove habitat
type, such that it uses its short siphons to feed on sus-
pended particles. In contrast, coastal and island zones
appeared to mostly favor the deposit feeders (worms and
crabs) of different sizes, which often feed on mangrove
leaves and detritus. Meanwhile, based on the results
of PERMANOVA analysis, the whole community was
not distinct from each other in either island or coastal
zones. However, a closer look at the crustacean popula-
tion unveiled the significant differences (island/coastal:
pseudo-F=2.75, P (perm) = 0.005) (Fig.3). In the man-
grove biotopes, Qureshi and saher (2012) found that abi-
otic characteristics such as substrate preference and tidal
periodicity (distance from the water mark during low
tide) can be affected in spatial variations and densities
of burrowing crabs. Indeed, various mangrove habitats
have different effects on the distribution and behavioral
adaptation of benthic macrofaunal species (Samidurai
etal. 2012; Thilagavathi etal. 2013). Furthermore, nMDS
ordination plot illustrated some separation between three
zones confirming the conclusion of PERMANOVA analy-
sis (Fig.4). The range of stress values was rather good
across the nMDS plot for the zones (0.13), indicating the
dissimilarity between the main faunal groups of each zone
(Clarke and Warwick 2001).
Diversity indices
To determine the diversity and distribution of species,
macrofaunal community indices were measured and the
results were discussed (Fig.5a–d). Deltaic zone tended
to have the highest total abundance (warm season,
1024 ± 587ind/m−2) among all the sampled stations, fol-
lowed by island zone, while coastal zone always had the
lowest abundance (warm season, 217 ± 123ind/m2) dur-
ing the study period (Fig.5a). The Shannon–Wiener index
(H) (Fig.5b) varied between 1.649 (coastal, warm season)
and 2.163 (deltaic, warm season). These moderate levels
of diversity values indicated that the macrofaunal com-
munity is under stress due to natural and/or anthropogenic
factors. The deltaic zone was found to be less negatively
influenced by the anthropogenic effects on the environ-
ment compared to the other zones, while the coastal zone
was found to be under more pressure caused by human
activities such as domestic waste and oil spills (especially
in summer). It was also found that the tides bring the solid
wastes from the fishing and port activities into the coastal
zone. The evenness component (J′) (Fig.5c) ranged from
0.438 (deltaic, cold season) to 0.957 (island, warm sea-
son). Species richness and total abundance gradually
decreased from the deltaic zone to the coastal zone, while
the species evenness slightly increased from the deltaic to
the coastal zone. The richness component (D) (Fig.5d)
varied between 0.336 (island, warm season) and 2.788
(deltaic, warm season).
0
200
400
600
Deltaic Island Coastal
Abundanc (ind/m-2)
Bivalvia
Gastropoda
Crustacea
Polychaeta
oligochaeta
abc
abc
aab
a,ab,b
a,ab,b
abc
aaa
aaa a,ab,b
aba
aaa aba
aaa
aba
aaa
Fig. 3 Mean (± SE) total abundance of Bivalvia, Gastropoda, Crus-
tacea, Polychaeta and Oligochaeta within three mangrove zones
(coastal, island and deltaic); different lower case letters indicate sig-
nificant differences between zones
Fig. 4 nMDS ordinations showing groupings in macrofaunal compo-
sition among different zones in the study area
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International Journal of Environmental Science and Technology
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Relationship betweenenvironmental variables
anddiversity ofbenthic macrofauna
Generally, a correlation was found between the variations
in the diversity or richness of macrobenthic faunal and
environmental variables (e.g., temperature and salinity;
Satheesh Kumar and Basheer Khan 2013; Libres 2015),
large-scale features of habitat (e.g., forest type; Linde-
garth and Hoskin 2001) or sediment texture (e.g., whether
it is sandy or muddy; Samidurai etal. 2012). In the pre-
sent study, the diversity index was positively correlated
with temperature (r = 0.64; p < 0.01) and was negatively
correlated with salinity (r = 0.50; p <0.05) in the deltaic
zone. The fluctuations of salinity had a profound influ-
ence on the species richness in the deltaic mangrove zone,
as it is located in the mouth of Mehran River. Salinity
acts as a major ecological factor in the distribution of
living organisms, and the variation in the salinity caused
by dilution and evaporation is most likely to influence the
faunal distribution of the coastal ecosystems (Mousavi
Nadushan and Mokhayer 2017). In this research, the first
two axes of the PCA ordination explained 99.11% of the
variance in species–environment relationships. Accord-
ing to the results, the eigenvalues for axes 1, 2, 3 and 4
were 0.948, 0.042, 0.005 and 0.002, respectively, and the
Fig. 5 Univariate measures for
macrobenthic macrofauna in the
study area. a Species abundance
(N), b Shannon–Wiener diver-
sity (H), c Pielou’s evenness (J),
d Margalef richness (D)
0
400
800
1200
Abundance (N)
A
cold
warm
0
0.5
1
1.5
2
2.5
delta Islandcoastal delta island coastal
Diversity (H)
B
cold
warm
0
0.2
0.4
0.6
0.8
1
Evenness(J)
C
cold
warm
0
0.5
1
1.5
2
2.5
deltaislandcoastal
delta Island coastal
Richness (D)
D
cold
warm
1.0-1.0
1.
0
-0.6
Como
Sacu Barb
Doce
Tepa
Assp
Ceci
Baam
Ucas
Ocys
Scol
Mage
Neph
Amph
Temperature
TOM
Silt+Clay
Sand
Salinity
Fig. 6 PCA ordination diagram displaying the position of the most
abundant taxa in relation to environmental variables best explaining
their distribution among sites; solid arrows represent the environmen-
tal vectors including temperature, salinity, TOM, silt–clay and sand;
the dashed arrows represent the invertebrate taxa; the arrows pointing
in the same relative direction are correlated, while longer arrows indi-
cate increasing values. Key to taxa: Como: Corbula modesta, Sacu:
Saccostrea cucullata, Barb: Barbatia sp, Doce: Dosinia ceylonica,
Tepa: Terebalia palustris, Assp: Asseminea sp, Ceci: Cerithidea cin-
gulata, Baam: Balanus amphitrite, Ucas: Uca spp, Ocys: Ocypode sp,
Scol: Scoloplos sp, Mage: Magelona sp, Neph: Nephtys sp
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International Journal of Environmental Science and Technology
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percentage of total explaining variance measured for PCA
was 41%. PCA plot revealed that Saccostrea cucullata,
Asseminea sp, Magelona sp, Scoloplos sp and Ocypode sp
are correlated with the temperature and salinity (Fig.6).
The results indicated that the sediment particle size with
longer arrows plays a significant role in the distribution
of some species in their natural habitats. For example,
PCA indicated that Balanus amphitrite is found in habi-
tats with the highest sand percentage, while Dosinia cey-
lonica is detected in habitats with the lowest percentage
of silt–clay.
In muddy intertidal habitats, benthic assemblages were
found to be strongly correlated with particular properties of
the sediment (Chapman and Tolhurst 2007; Anderson 2008),
although some studies found no or relatively weak relation-
ships (Wu and Shin 1997; Barnes and de Villiers 2000).
Other studies suggested that organization of benthic assem-
blages in soft bottom may be primarily influenced by the
predation, physical disturbance (Thrush and Dayton 2002),
pollution or colonization-associated factors (Lundquist etal.
2006). In this study, the sediment particle size, tempera-
ture and salinity were the main environmental factors which
seem to have affected the distribution of the macrofaunal
species.
Conclusion
Mangroves have been extensively investigated for decades
by the ecologists and marine scientists. Mangrove forests
are complex environments including different kinds of
habitats, with various macro-invertebrate taxa living on or
in the sediments. In south of Iran, mangroves mostly occur
in estuaries. Meanwhile, there is rare evidence regarding
the ecological aspects of these habitats in recent years. The
results of the current study on macrobenthic community
composition within mangrove stands (i.e., deltaic, coastal
and island zones) at Hara Biosphere Reserve revealed that
the deltaic zone has a high density and diversity of macro-
fauna, while coastal habitats have the lowest densities and
diversities among all the studied zones studied. It could be
concluded that the different hydrological conditions, tem-
perature, salinity and sediment texture are the major fac-
tors significantly affecting the dispersion of macrofaunal
community in the mangrove habitats. The results of this
study provided the substantial evidence regarding the role
of distinctive habitats in the biodiversity and food webs of
mangrove stands, which can be compared with the findings
of the future studies to monitor environmental changes
and show the process of improvement or degradation of
the system. It also allows the resource managers to assess
the ecological value of these ecosystems and evaluate the
effects of environmental decisions. Evidently, such ecolog-
ical studies need to be replicated at multiple spatial scales
to provide further insights into the differences of these
habitats. Since the relationships between environmental
variables and spatial patterns of benthic assemblages are
complicated in mangrove ecosystem, it is recommended
to consider the effect of other factors (e.g., BOD content,
turbidity and nutrients) responsible for fluctuation in ben-
thic macrofaunal communities.
Acknowledgments We would like to thank Tehran University and
Sciences and Researches University for supporting this study. Many
thanks for the accommodation provided by M. Sharifi and the boat trips
provided by Dr. Shirvani. Our sincere gratitude goes to Dr. Shokri and
Dr. Ghaziloo at Shahid Beheshti University, who guided us through
statistical analysis and editing this manuscript.
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