Regional Studies in Marine Science 32 (2019) 100826

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Regional Studies in Marine Science

journal homepage: www.elsevier.com/locate/rsma

Community composition and diversity of phytoplankton in relation to

environmental variables and seasonality in a tropical mangrove
estuary
∗
A.S.M. Saifullah a,b , , Abu Hena Mustafa Kamal a,c , Mohd Hanafi Idris a,c ,
Amy Halimah Rajaee a
a
Department of Animal Science and Fishery, Universiti Putra Malaysia Bintulu Sarawak Campus, 97008 Bintulu, Sarawak, Malaysia
b
Department of Environmental Science and Resource Management, Mawlana Bhashani Science and Technology
University, Santosh-1902, Tangail, Bangladesh
c
Faculty of Fishery and Food Sciences, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia

article info a b s t r a c t

Article history: This paper presents the aspects of phytoplankton communities along a tropical mangrove estuary in
Received 2 September 2018 Sarawak, Malaysia. Data were collected monthly from the study area from January 2013 to December
Received in revised form 29 July 2019 2013 and was pooled into seasons to examine the influence of seasonality. The estuary revealed
Accepted 6 September 2019
relatively species-rich, and a total of 102 species under 43 genera were recorded comprising 6 species
Available online 12 September 2019
of Cyanophyceae; 4 species of Chlorophyceae; 62 species of Bacillariophyceae and 30 species of
Keywords: Dinophyceae. The species composition, as well as the mean abundance (cellsL-1) of phytoplankton,
Phytoplankton community were found in order of Bacillariophyceae>Dinophyceae> Cyanophyceae> Chlorophyceae. Mean abun-
Environmental variables dance of phytoplankton ranged from 5694 to 88890 cellsL−1 over the study period with its higher
Seasonality value in the dry season. Species recorded from the estuary were dominated by Pleurosigma normanii,
Tropical mangrove estuary Coscinodiscus sp, Coscinodiscus centralis, Coscinodiscus granii, Dinophysis caudata, Ceratium carriense,
Ceratium fusus, and Ceratium lineatum. Abundance of phytoplankton demonstrated positive correlation
with chlorophyll a (r=0.69), ammonium (r=0.64) and silica (r=0.64). Significant differences (ANOSIM
and nMDS) were observed in the species community structure between intermediate and the wet
season. Canonical correspondence analysis (CCA) showed that most of the species assemblages were
positively correlated with surface water temperature, salinity, pH, ammonium and nitrate in the
intermediate and dry season towards larger species composition in the respective seasons whereas
silica showed influence on the species assemblage in the wet season. The findings suggest that the
Sibuti mangrove estuary is productive in terms of diversified phytoplanktons and their variability in
assemblage, those are influenced by the hydrological and biological factors.
© 2019 Elsevier B.V. All rights reserved.

1. Introduction through the productivity of the phytoplankton and zooplankton

as primary and secondary producers. However, the availability
Phytoplanktons are free floating tiny floral components that of phytoplankton influences the distribution of consumer organ-
are widely distributed in the marine and estuarine environments. isms, like immediate herbivore zooplankton and creates an active
They play an important role to make the estuarine ecosystem link in the food chain. Phytoplankton contains a high nutrient
more productive. These microscopic organisms are vital and im- which enables them valuable food item in the aquatic food chain
portant as a primary producer and source of food supply to the (Khatoon et al., 2009; Lim et al., 2014).
aquatic body. Phytoplankton are also one of the initial biological The mangrove estuaries are known as a highly productive and
components from which the energy is transferred to higher or- essential ecosystem for fisheries in the tropical region (Saifullah
ganisms through the food chain (Tiwari and Chauhan, 2006). Fer- et al., 2015). Faunal communities in mangrove ecosystems have
tility and healthiness of the mangrove environment are reflected traditionally been considered to be driven by the large production
of mangrove litter (Odum and Heald, 1975), though recently
∗ Corresponding author at: Department of Environmental Science and Re- several studies have shown that the importance of phytoplankton
source Management, Mawlana Bhashani Science and Technology University, and benthic microalgae may have been underestimated in this
Santosh-1902, Tangail, Bangladesh. ‘detritus-based foodweb’ concept (Newell et al., 1995; Loneragan
E-mail address: asmsaifullah@mbstu.ac.bd (A.S.M. Saifullah). et al., 1997). The distribution and abundance of commercially

https://doi.org/10.1016/j.rsma.2019.100826
2352-4855/© 2019 Elsevier B.V. All rights reserved.
2 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826

important fish and shellfish and their larvae are dependent on mouth of the river is around 150 m wide and shallow with
some species of the phytoplankton besides serving as their main an average depth of 5 m. There exists sandbank in one side
food source (Mitra et al., 2004). apparently due to the deposition of sand caused by tidal currents.
There also exist interlinkages between phytoplankton and Sibuti mangrove estuary is margined in both sides by Rhizophora
zooplankton community composition where change in phyto- apiculata and Nypa fruticans. The estuary is semi-diurnal and
plankton community composition can influence the food web tidal range varied between 0.2 to 2.1 m during neap and spring
structure and energy flow in the pelagic ecosystem (KiØrboe, tide, respectively (DOMSM, 2013). Samplings were done monthly
1996). The abundance, distribution, and species composition data from January 2013 to December 2013 in three stations, viz. 1, 2
of phytoplankton are important for the study of estuarine ecosys- and 3 located at 3◦ 59′ 25.76′′ N and 113◦ 43′ 51.6′′ E; 3◦ 58’53.5′′ N
tems. It is reported that phytoplankton species undergoes spa- and 113◦ 44′ 12.12′′ E and 3◦ 59′ 22.24′′ N and 113◦ 44′ 35.33′′ E, re-
tiotemporal changes in their distribution due to the different spectively. Collected monthly data were pooled into seasons.
effects of hydrographical factors on individual species (Rajku- The seasonal cycle in Malaysia is divisible into three distinct
mar et al., 2009). The production of phytoplankton is largely categories, viz. (1) wet season (September to December), (2) in-
dependent on the nutrient concentrations and light availabil- termediate (January to April) and (3) dry season (May to August)
ity in the photic zone (Yusoff, 1989). In addition to light and (Saifullah et al., 2014).
oxygen, phytoplankton requires basic simple inorganic chemical
nutrients, like phosphate nitrate (NO3 − ), (PO4 − ), carbon dioxide 2.2. Sampling
(CO2 ), and some diatoms require a form of silicon (SiO4 − ) for their
growth and sustenance (Verlencar and Desai, 2004). The changes 2.2.1. Collection of water sample and analysis
in the structure of the phytoplankton community can be influ- In-situ data for water pH, temperature, salinity, turbidity, con-
enced by their surrounding environment in ways which favour ductivity and dissolved oxygen (DO) were determined in three
or disfavour their continued persistence (Rahman et al., 2013). replicates for each station using water quality metre (WQC-24,
Phytoplankton community and size composition are also known DKK-TOA Corporation, Japan). Secchi depth was measured by
to be related to nutrient availability (Cushing, 1989). Nutrient Secchi disc (30 cm diameter), and light extinction coefficient
enrichment can be predicted to alter phytoplankton community (LEC) was calculated according to Boyd (2000). Corresponding air
composition (Sprules and Munawar, 1986; Kimor, 1992; Huszar temperature and rainfall data for the study area were collected
et al., 1998; Saifullah et al., 2014). However, several studies have from Meteorological Department of Malaysia (DOMSM, 2013).
unveiled that physical and chemical variables have pronounced For analysis of water nutrients, three replicates of surface water
influence on plankton communities in mangrove waters than the samples for each station were collected in pre-washed polyethy-
nearshore coastal environment, resulting in seasonal changes of lene bottles and was kept in the icebox followed by immediate
plankton species composition and densities (Kannan and Vasan- shifting to the laboratory. The water samples were filtered using
tha, 1992). Thus, the estimation of those physical parameters and Millipore filtering system (MFS) and analysed for dissolved inor-
inorganic chemicals is also essential for studying the community ganic phosphate, nitrate and ammonium following the methods
structure of phytoplankton in an aquatic environment. of Parsons et al. (1984), Kitamura et al. (1982) and Weatherburn
Approximately 4000 species of marine phytoplankton have (1967) respectively. The content of silica in the water sample
been described, and new species are continuously being added to was determined using Silicomolybdate method (HACH, 8185).
this total (Lalli and Parsons, 1997), but there reveals no specific Chlorophyll a concentration was estimated following the method
value for the phytoplankton composition in the estuarine regime. described by Coombs and Hall (1982).
Different observations on phytoplankton abundance and distri-
bution were conducted in the area of the Gulf of Thailand and 2.2.2. Collection and analysis of phytoplankton sample
in the east coast of Peninsular Malaysia (Rose, 1926; Boonyapi- Three replicate samples of phytoplankton were collected from
wat, 1983; Suvapepun, 1979 and Piromnim, 1984). Studies on the surface water by horizontal towing of plankton net (0.35
phytoplankton communities in mangrove estuaries are limited in m mouth diameter) of bolting silk (mesh size of 20 µm) in
Malaysia. One of the country’s priority fishery areas of Sarawak each sampling. The samples were preserved in 5% neutralized
region is a very good mangrove estuarine ecosystem, but scarcely formalin for further analysis. The volume of water filtered by the
studied the ecology of this regime. In this line, Sibuti mangrove net was estimated by the cylinder formula (Newell and Newell,
estuary has been recognized as a very productive estuary ac- 1977). Numerical analysis was done using a Sedgwick rafter cell
cording to its water quality (Saifullah et al., 2014; Hoque et al., counter under a compound microscope following the method
2015). It is also hypothesized that the Sibuti mangrove estuary described by Newell and Newell (1973) and Sukhanova (1978).
would be a good harbour of diverse phytoplankton species. Thus, Phytoplankton was identified following the standard methods of
phytoplankton study in the waters of the mangrove dominated Taylor (1976), Hustedt (1930) and Cupp (1943).
estuarine area of Miri, Sarawak is necessary for a better under-
standing of the hydrographic feature and its influence on the 2.3. Statistical analysis
organisms around this mangrove ecosystem.
This study encompasses the investigation of community struc- Results were calculated as the mean value of the triplicate
ture, abundance, and seasonal distribution of phytoplankton tests with the standard deviation. One-way ANOVA was carried
in Sibuti mangrove estuary and the outcome of which would be out to determine the seasonal variations of different hydrobio-
able to indicate the productivity of the estuary. logical factors. Biodiversity indices (Shannon–Wiener diversity,
Margalef species richness, Pielou’s species evenness) and catch
2. Materials and methods composition of different fishery resources were compared using
the statistical application software, SAS (version 9.2). Pearson’s
2.1. Study area correlation coefficients were performed using Community Anal-
ysis Package (CAP) software (version 4.0). The Shannon–Wiener
The Sibuti mangrove estuary (SME) is located in the tropi- diversity Index (H′ ), Margalef species richness (D) and species
cal region of Malaysia (Fig. 1). The river opens into the South evenness (J) were determined using the PRIMER software pack-
China Sea and bounded by Bungai farmlands on the north. The age (version 5.0). Non-metric multidimensional scaling (nMDS;
 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826 3

Fig. 1. Map of study area and sampling stations at Sibuti Mangrove Estuary (SME).

a mostly two-dimensional diagram) was used for the purpose (5.01 ± 2.65 PSU). Salinity also showed positive correlation with
of showing and determining the seasonal similarities and dis- TDS, pH, conductivity and negative co. Dissolved oxygen ranged
similarities of species assemblages. Two-dimensional nMDS was from 1.94 to 6.71 mg L−1 during the study period. However, the
generated based on the species composition found in each season. maximum mean value of DO was observed in the dry season
ANOSIM (Analysis of similarity) was used to evaluate the degree (4.5 ± 1.25 mg L−1 ) and minimum in the intermediate season
and significance of the nMDS (Paramo et al., 2012). ANOSIM (3.29 ± 0.49 mg L−1 ) (Table 1). DO revealed positive correlation
(Clarke, 1993) output is a sample statistic (global R); if the output with TDS (Table 2). The TDS value in the estuary ranged from 0.5
is equivalent to 1, there is strong dissimilarity between two as- to43.9 mg L−1 for the whole study period. Meanwhile, the highest
semblages, while if it is 0, there is no dissimilarity found between mean of TDS was observed in the dry season (26.58 ± 7.43 mg
two assemblages (Paramo et al., 2012). The dendrogram shows L−1 ) and the lowest in the intermediate season (7.06 ± 4.50
the similarities of species assemblages in each season in terms mg L−1 ) (Table 1). The highest mean value of conductivity was
of abundance (number of species caught in all nets in one time) observed in the dry season (2.91 ± 0.53 S/m) followed by the
using the Bray–Curtis similarity index. Similarity percentage anal- intermediate and wet season (Table 1). The maximum mean of
ysis (SIMPER) was used to determine the contributory as well as LEC (K) was found in the intermediate season (2.68 ± 0.77) and
discriminating species in each season. Canonical correspondence minimum in the dry season (2.33 ± 0.69). Significant seasonal
analysis (CCA) was used to observe the influence of hydrobiologi- variations were observed among some hydrological parameters
cal factors on the species composition of fishery resources. Before such as surface water temperature (df = 2, f = 105.07, P =
accomplishing these multivariate analyses, species assemblages <0.0001), salinity (df = 2, f = 37.90, P = 0.0004), TDS (df =
data were logarithmically transformed [log10 (x + 1)] to re- 2, f = 62.12, P = <.0001) and conductivity (df = 2, f = 28.25,
duce the variance (Zar, 1996). Multivariate analyses were carried P = 0.0009). Wherever, no seasonal variations were found for
out using CAP (Community Analysis Packages, version 4.0), and pH (df = 2, F = 0.35, P = 0.76) and DO (df = 2, f = 3.08,
CCA was conducted using CANOCO for Windows 4.5 (Seaby and P=0.12)(Table 1).
Henderson, 2007). The mean concentration of nitrate (NO3 ) was found to be
higher in the wet season (1.51 ± 0.85 mg L−1 ) lower in the dry
2.4. Results (1.20 ± 0.42 mg L−1 ) and intermediate (0.86 ± 0.28) season.
Phosphate (PO4 ) concentration was higher in the intermediate
2.4.1. Environmental variables and wet seasons (0.27 ± 0.28 mg L−1 ), whereas it was found to be
The air temperature of the study area varied between 32.2 ◦ C lower in the wet season (0.06 ± 0.02) (Table 1). The concentration
and 33.6 ◦ C with the highest in the dry season and the lowest of Phosphate showed positive correlation with LEC (Table 2). The
in the wet season. The average monthly rainfall in the area was mean value of ammonium (NH4 ) demonstrated higher concen-
316.17 mm during the study period. The surface water tempera- tration in the dry (1.04 ± 0.11 mg L−1 ) season followed by the
ture of the estuary ranged from 27.1 ◦ C to 32.2 ◦ C. The maximum intermediate (0.65 ± 0.41 mg L−1 ) season. Ammonium demon-
mean surface water temperature was observed in the dry sea- strated positive correlation with salinity (Table 2). Silica (SiO2 )
son (30.52 ± 1.21 ◦ C) and minimum in the wet season (27.95 was found to be higher in the intermediate season (2.68 ± 0.78
± 0.90 ◦ C) (Table 1). Surface water temperature demonstrated mg L−1 ) and lower in the dry season (2.41 ± 0.60 mg L−1 ). The
significant positive correlation with air temperature, salinity and chlorophyll a concentration of the surface water was higher in
negative correlation with LEC and rainfall (Table 2). The overall the intermediate season (0.14 ± 0.09 mgm−3 ) and lower in the
pH values during the study period ranged from 4.41 to 7.35 with dry and wet season (0.03 ± 0.01 mg m−3 ).
its maximum value in the dry season (6.66 ± 0.55) and mini- The concentrations of NH4 (df = 2, f = 1.92, p = 0.00017) and
mum in the intermediate season (5.84 ± 0.43) (Table 1). There chlorophyll a (F = 15.54, P = < 0.0042) varied with the seasons.
revealed a significant positive correlation among pH, salinity and However, no seasonal variations were found for NO3 (df = 2, f =
conductivity (Table 2). Salinity ranged from 0.3 to 27.1 PSU for 2.56, P = 0.15), PO4 (df = 2, f = 1.74, P = 0.25) and silica (df =
the whole study period. Maximum mean salinity was found in the 2, f = 0.75, P = 0.56).
dry season (18.76 ± 2.48 PSU) and minimum in the wet season
 4
A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826
Table 1
Seasonal mean values of different hydrological parameters recorded in different seasons during the study period in SME.
Parameter
Season SWT pH Salinity DO TDS Conductivity LEC NO3 PO4 NH4 Silica Chl a
(o C) (PSU) (mg L−1 ) (mg L−1 ) (S/m) (K) (mg L−1 ) (mg L−1 ) (mg L−1 ) (mg L−1 ) (mg L−1 )
Inter 28.48 ± 1.16b 5.84 ± 04.3a 5.73 ± 4.96b 3.29 ± 0.49a 7.06 ± 4.50b 0.94 ± 0.40b 4.51 ± 1.84a 0.86 ± 0.28a 0.27 ± 0.14a 0.65 ± 0.41c 2.68 ± 0.78a 0.14 ± 0.09a
Dry 30.52 ± 1.21a 6.66 ± 0.55a 18.76 ± 2.48a 4.5 ± 1.25a 26.58 ± 7.43a 2.91 ± 0.69a 2.50 ± 0.92c 1.20 ± 0.42a 0.09 ± 0.09a 1.04 ± 0.11a 2.41 ± 0.60a 0.08 ± 0.06a
Wet 27.95 ± 0.90c 5.85 ± 0.26a 5.01 ± 2.65b 4.16 ± 0.69a 8.10 ± 3.53b 2.59 ± 0.72b 3.85 ± 0.87b 1.51 ± 0.85a 0.06 ± 0.02a 0.67 ± 0.34a 2.59 ± 0.72a 0.03 ± 0.01b

Different letters (within the columns) indicate a significant difference between means using Tukey’s test at p≤ 0.05; SWT = Surface water temperature; LEC = Light extinction coefficient.
 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826 5

2.4.2. Community composition and abundance of phytoplankton

One hundred two (102) species of phytoplankton were identi-
fied from the Sibuti mangrove estuary. The identified phytoplank-
ton comprised of 43 genera under 4 divisions i.e. Cyanophyta
(Blue–green algae), Diatom (Bacillariophyceae), Dinoflagellate
(Dinophyceae) and Chlorophyta (Chlorophyceae). Out of 102
species, 6 species were from Cyanophyceae; 4 species from
Chlorophyceae; 62 species from Bacillariophyceae and 30 species
from Dinophyceae (Table 3). The major portion (62%) of the
total phytoplankton was occupied by Bacillariophyta (Diatom)
followed by dinophyta or dinoflagellates (28%), Cyanophyta (6%)
and only 4% of the Chlorophyta. The percent composition of each
group of phytoplankton was found in the order of Diatom >
Dinoflagellate > Cynaophyceae > Chlorophyceae.
Cyanophyta comprised only 6 species viz. Anabaena sp., An-
abaena affinis, Calothrix sp., Oscillatoria erythraea, Oscillatoria Fig. 2. Seasonal variation of total phytoplankton abundance in SME during the
limosa, and Oscillatoria sp. However, the occurrence of Cyanophyta study period.
was patchy and mostly dominated by Anabaena sp. and least
abundant species was Calothrix sp. found only in January, whereas
Anabena affinis was observed in November and December. Chloro-
phyta comprised the least number of species and was dominated
by Spirogyra sp. (Table 3)
Diatoms were dominated by Rhizosolenia spp. comprising 8
species viz. Rhizosolenia alata, Rhizosolenia imbricata, Rhizosole-
nia clevei, Rhizosolenia curvata, Rhizosolenia robusta, Rhizosole-
nia stolterforthii, Rhizosolenia styliformis followed by 6 species
of Coscinodiscus spp. including Coscinodiscus granii, Coscinodiscus
centralis, Coscinodiscus jonesianus, Coscinodiscus radiatuss, Coscin-
odiscus sp., and Coscinodiscus thorii (Table 3).
Among 29 species of Dinophyceae (Dinoflagellate), Ceratuium
spp. dominated with 12 species (41.37% of dinoflagellates) viz.
Ceratium carriense, Ceratium furca, Ceratium fusus, Ceratium hor-
ridum, Ceratium lineatum, Ceratium macroceros, Ceratium paradox- Fig. 3. Non-metric Multidimensional Scaling (n-MDS) ordination of phytoplank-
ides, Ceratium trichoceros, Ceratium tripos, Ceratium vulture, Cer- ton community in different months grouped into seasons during the sampling
atium breve followed by Dinophysis spp.(17% of dinophyta) with 5 period.
species including Dinophysis caudata, Dinophysis hastata, Dinoph-
ysis fortii, Dinophysis miles, Dinophysis sp. and Protoperidinium spp.
(13.79% of dinophyta) comprised of 4 species viz. Protoperidinium carriense whereas, Thalassionema nitzschioides, Nitzschia sp., Cer-
depressum, Protoperidinium divergents, Protoperidinium sp., and atium fusus, Chaetoceors pseudocurvisetus, Oscillatoria sp., Dinoph-
Protoperidimium Oceanicum (Table 3). ysis caudata, Rhizosolenia imbricata, Ceratium carriense. Whereas,
The abundance of phytoplankton was higher in the dry season Nitzschia sp., Bacillaria paradoxa, Rhizosolenia clevei, Tetradinium
ranged from 31078.89 to 67594.66 cells L−l (48,727.24 cells L−l ) javanicum, Ceratium furca, Ditylum brightwelli, and Thalassionema
followed by the intermediate ranging from 30176 to 57380.84 nitzschioides were the most discriminatory species observed be-
cells L−1 (42,891.19 cells L−1 ), and in the wet season ranged from tween the intermediate and the wet season.
15691.61 to 30455.57 cells L−1 (23,109.57 cells L−1 ) (Fig. 2). The The SIMPER revealed the succession of individual species in
abundance of phytoplankton showed positive correlation with different seasons (Table 4). The highest average similarity in
Chl a (Table 2). The phytoplankton density in different stations species composition was observed in the wet season (49.28%)
varied with ranges from 19436–88890 cells L−1 (station 1), 8480– followed by an intermediate and the dry season (Table 5). The
87526 cells L−1 (station 2) and 5694–52986 cells L−1 (station 3). contribution of species varied from season to season, wherein
However, no significant variation of abundance was found among the intermediate season the highest contributory species was
the stations (df = 2, f = 4.09; p = 0.028) or among the seasons Coscinodiscus granii (10.66%) whereas in the dry season Biddulphia
(df = 4, f = 0.24, p = 0.912)(see Fig. 3). mobiliensis showed the highest contribution (13.81%). The nMDS
(Fig. 3) also showed significant influence of seasonality (2D stress
2.4.3. Species assemblage = 0.91) on the assemblage of phytoplankton.
The SIMPER and ANOSIM were employed to observe the sea-
sonal variation in species composition. The SIMPER analysis 2.4.4. Species diversity, richness, and evenness
showed the dissimilarity or variation of species assemblages The Shannon–Wiener diversity index (H′ ) of phytoplankton
between two seasons (Table 3). The highest average dissimi- ranged from 2.55 to 3.53 for the whole study period. The diversity
larity was found between the intermediate and the wet sea- index (H′ ) was found to be higher in the intermediate season
son (65.17%), whereas the lowest was found between the dry ranging from 2.99 to 3.23 (3.13), while the lower index was ob-
and the wet (56.90%) season (Table 4). The major discriminat- served in the wet season ranging from 2.91 to 3.21 (3.07) (Fig. 4a).
ing (1.69–2.44% contribution) species found between the dry The overall diversity (H′ ) for all seasons was 3.10. Spatially, the
and the intermediate seasons were Thalassionema nitzschioides, diversity index (H′ ) was found in an order of station 2 > station 1
Nitzschia sp., Ceratium fusus, Chaetoceors pseudocurvisetus, Oscilla- > station 3 (Fig. 4a). The highest species richness (d) was found in
toria sp., Dinophysis caudate, Rhizosolenia imbricate and Ceratium the dry season ranging from 2.36 to 2.78 (2.51), and the lowest
6 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826

Table 2
Pearson correlation coefficient among environmental parameters, water nutrients, chlorophyll a and phytoplankton abundance in Sibuti mangrove estuary
(n = 15).
AT WT Rainfall pH TDS Sal. DO Cond. NO3 PO4 NH4 Si Chl a LEC Phyto
AT 1 0.692∗ −0.511 0.304 0.377 0.480 −0.152 0.486 −0.329 0.079 0.495 0.404 0.185 −0.557 0.402
WT 0.692∗ 1 −0.250 0.473 0.708∗ 0.744∗∗ 0.119 0.776∗∗ −0.307 −0.272 0.376 −0.058 0.182 −0.776∗∗ 0.287
Rainfall −0.511 −0.250 1 −0.570 −0.524 −0.630∗ −0.333 −0.566 −0.109 0.050 −0.620∗ −0.113 −0.118 0.266 −0.644**
pH 0.304 0.473 −0.570 1 0.832∗∗ 0.843∗∗ 0.533 0.726∗∗ 0.044 −0.358 0.524 −0.252 0.107 −0.480 0.531
TDS 0.377 0.708∗ −0.524 0.832∗∗ 1 0.951∗∗ 0.596∗ 0.941∗∗ 0.052 −0.268 0.575 −0.237 0.146 −0.623∗ 0.412
Sal 0.480 0.744∗∗ −0.630∗ 0.843∗∗ 0.951∗∗ 1 0.451 0.972∗∗ 0.022 −0.331 0.600∗ −0.134 0.095 −0.678∗ 0.530
DO −0.152 0.119 −0.333 0.533 0.596∗ 0.451 1 0.414 0.564 −0.083 0.089 −0.382 −0.215 −0.136 0.027
Cond. 0.486 0.776∗∗ −0.566 0.726∗∗ 0.941∗∗ .0972∗∗ 0.414 1 −0.041 −0.200 0.522 −0.130 0.068 −0.644∗ 0.244
NO3 −0.329 −0.307 −0.109 0.044 0.052 0.022 0.564 −0.041 1 −0.169 0.068 −0.077 −0.232 −0.051 0.014
PO4 0.079 −0.272 0.050 −0.358 −0.268 −0.331 −0.083 −0.200 −0.169 1 −0.477 0.117 −0.026 0.592∗ −0.118
NH4 0.495 0.376 −0.620∗ 0.524 0.575 0.600∗ 0.089 0.522 0.068 −0.477 1 0.275 0.383 −0.630∗ 0.645**
Si 0.404 −0.058 −0.113 −0.252 −0.237 −0.134 −0.382 −0.130 −0.077 0.117 0.275 1 −0.051 −0.196 0.644**
Chl a 0.185 0.182 −0.118 0.107 0.146 0.095 −0.215 0.068 −0.232 −0.026 0.383 −0.051 1 −0.234 0.692**
LEC −0.557 -.776∗∗ 0.266 −0.480 −0.623∗ −0.678∗ −0.136 −0.644∗ −0.051 0.592∗ −0.630∗ −0.196 −0.234 1 0.136
Phyto 0.402 0.287 −0.644** 0.531 0.532 0.530 0.027 0.244 0.014 −0.118 0.645** 0.644** 0.692** 0.136 1

Sal = Salinity; Tem = Temperature; Con = Conductivity; Nit = Nitrogen; Am = Ammonium Sil = Silica; Chla = Chlorophyll a; Phy = Phytoplankton. ** Correlation
is significant at the 0.01 level (2-tailed). * Correlation is significant at the 0.05 level (2-tailed).

Fig. 4. Seasonal (a) diversity, (b) richness and (c) evenness of phytoplankton species in Sibuti mangrove estuary.

was in the intermediate season ranging from 2.6 to 2.52 (2.49), p = 0.955). There was also revealed no significant difference in
and the overall richness (d) revealed 2.50. While, species richness species richness (d) among stations (f = 1.40, p = 0.262); seasons
was higher in station 1 followed by station 2 and 3 (Fig. 4b) (f = 0.01, p = 0.992) and stations vs seasons (f = 0.26, p = 0.901).
and the overall mean of species richness (d) was 2.50. Whereas, The evenness (J́) measures for the phytoplankton species also did
species evenness (J′ ) was observed very close among the seasons not show any significant difference among stations (f = 2.07; p
e.g., 0.95, 095 and 0.93 in the intermediate, wet and dry season = 0.145); seasons (f =1.64, p = 0.212) and among stations vs
respectively. Similarly, spatial variation was also observed very seasons (f = 0.33, p = 0.853).
minimal (Fig. 4c). Canonical correspondence analysis (CCA) revealed eigenval-
Analysis of variance (ANOVA) for diversity index did not reveal ues of 0.345, 0.283, 0.233, and 0.214 at axis 1, 2, 3, and 4
any significant difference among stations (f = 3.23, p = 0.055); respectively based on the p-value of 0.254 for all canonical axes.
seasons (f = 0.16, p = 0.856) or stations vs seasons (f = 0.16, Phytoplankton distribution and species abundance pattern are
 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826 7

Table 3
List of phytoplankton species recorded in Sibuti mangrove estuary with their seasonal mean abundance, annual
mean abundance, occurrence frequency (%F) and relative abundance (RA).
Code Species/Taxa Seasonal mean abundance (Cells L−1 ) Mean %F RA
abundance
(cells L−1 )
Intermediate Dry Wet
Cyanophyceae
1 Anabaena sp. 41.25 742.80 753.11 512.39 58.33 1.32
2 A. affinis 0 0 134.11 44.70 16.67 0.11
3 Calothrix sp. 123.79 0 0 41.26 8.33 0.11
4 Oscillatoria erythraea 371.4 61.9 0 144.43 25 0.37
5 O. limosa 0 257.91 0 85.972 8.33 0.22
6 O. sp. 526.13 0 226.96 251.03 41.67 0.65
Chlorophyceae
7 Chlorella sp. 0 0 453.93 151.31 16.67 0.39
8 Spirogyra sp. 1031.62 402.35 299.18 577.72 41.67 1.49
9 Closterium sp. 526.12 0 72.22 199.45 16.67 0.51
10 Pediastrum simplex 0 0 247.60 82.53 16.67 0.21
Bacillariophyceae (Diatom)
11 Actinocyclus sp. 134.11 0 0 44.705 8.33 0.11
12 Asterionella japonica 0 0 72.22 24.07 8.33 0.06
13 Bacillaria paradoxa 0 500.35 938.81 479.72 50 1.23
14 Bacteriastrum. delicatulum 0 660.25 0 220.08 16.67 0.57
15 B. hyalinum 0 20.63 0 6.878 8.33 0.02
16 B. sp. 206.32 0 0 68.78 8.33 0.17
17 Biddulphia granulata 0 10.32 0 3.44 8.33 0.008
18 B. mobiliensis*** 618.96 2187.09 577.72 1127.92 75 2.90
19 B. sinensis 0 0 247.6 82.53 8.33 0.21
20 Chaetoceors pseudocurvisetus 1227.65 1464.95 226.97 973.19 50 2.51
21 C. radicans 20.63 0 0 6.88 8.33 0.01
22 C. affinis 649.93 309.5 309.5 422.98 33.33 1.10
23 C. coarctatus 588.02 0 0 196.01 16.67 0.50
24 C. decipiens 618.96 2187.09 577.72 1127.92 75 2.90
25 C. furcatum 0 10.32 206.33 72.23 16.67 0.18
26 C. sp. 0 0 206.33 68.78 8.33 0.18
27 Coscinodiscus granii 1856.96 1227.67 835.64 1306.76 83.33 3.36
28 C. centralis 1991.08 1083.24 876.91 1317.08 75 3.39
29 C. jonesianus 0 990.39 495.20 495.19 41.67 1.27
30 C. radiatus 0 319.8 0 106.6 8.33 0.27
31 C. sp. 1609.35 1650.65 1072.91 1444.30 91.67 3.72
32 C. thorii 536.45 1176.09 433.3 715.28 50 1.84
33 Climacodium biconcavum 0 51.58 0 17.19 8.33 0.04
34 Ditylum brightwelli 1072.90 0 0 357.63 25 0.92
35 D. sol 216.64 1124.51 330.13 557.09 66.67 1.43
36 Eucampia zodiacus 577.71 422.98 0 333.56 25 0.86
37 Fragillaria oceanica 0 10.31 0 3.44 8.33 0.008
38 Gyrosigma sp. 72.21 61.9 0 44.70 16.67 0.11
39 G. spencerii 0 82.53 0 27.51 16.67 0.07
40 Hyalodiscus sp. 784.05 773.73 1021.33 859.70 75 2.21
41 Melosira sp. 0 711.84 196.01 302.62 33.33 0.78
42 Navicula sigma 0 30.94 371.40 134.11 25 0.34
43 Navicula sp. 257.9 257.9 371.40 295.73 33.33 0.76
44 Nitzschia sigma 350.75 0 226.96 192.57 16.67 0.50
45 Nitzschia sp. 1764.07 1660.95 0 1141.67 58.33 2.94
46 Odontella sinensis 309.48 1475.28 371.40 718.72 66.67 1.85
47 O. mobileinsis 0 0 443.61 147.87 16.67 0.38
48 O. sp. 330.12 113.48 402.33 281.98 33.33 0.73
49 Pleurosigma intermedium 0 422.98 0 140.00 8.33 0.36
50 Pleurosigma sp. 0 412.66 0 137.55 8.33 0.35
51 Pleursigma normanii 1165.75 1991.10 1186.40 1447.75 83.33 3.72
52 Proboscica alata 0 392.03 0 130.68 8.33 0.34
53 Pseudosolenia calcar-avis 0 0 41.26 13.75 8.33 0.03
54 Rhizosolenia alata 887.2 649.92 794.38 777.17 66.67 2.00
55 R. imbricata 660.24 175.38 567.41 467.68 58.33 1.20
56 R. polydactyla 763.4 1011.02 773.74 849.38 75 2.19
57 R. clevei 1176.03 1000.57 0 725.54 50 1.87
58 R. curvata 1093.55 1000.69 474.57 856.27 50 2.20
59 R. robusta 402.32 288.85 0 230.39 25 0.59
60 R. stolterforthii 0 30.95 0 10.32 8.33 0.03
61 R. styliformis 918.14 567.41 278.55 588.03 50 1.51
62 Skeletonema costatum 412.64 1083.23 1083.22 859.70 75 2.21
63 Thalassiosira costatum 41.25 0 0 13.75 8.33 0.03
64 T. sp. 557.05 0 0 185.68 16.67 0.49
(continued on next page)
8 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826

Table 3 (continued).
Code Species/Taxa Seasonal mean abundance (Cells L−1 ) Mean %F RA
abundance
(cells L−1 )
Intermediate Dry Wet
65 Thalassionema. frauenfeldii 959.42 1059.17 350.75 789.78 41.67 2.03
66 T. nitzschioides 701.5 629.25 1165.77 832.17 50 2.14
67 T. sp. 268.22 299.18 0 189.13 16.67 0.49
68 Thalassiothrix longissima 61.90 113.48 0 58.46 16.67 0.15
69 Triceratium favus 505.5 1341.16 257.9 701.52 33.33 1.81
70 T. javanicum 0 907.86 0 302.62 16.67 0.80
71 T. sp. 969.75 0 0 323.25 16.67 0.83
72 T. distinctum 273.37 422.98 0 232.11 16.67 0.60
Dinophyceae (Dinoflagellate)
73 Amphisolenia bidentata 226.96 412.66 0 213.21 25 0.55
74 Ceratium carriense 825.31 1372.10 453.91 883.77 58.33 2.27
75 C. furca 1155.41 412.66 51.86 539.98 58.33 1.39
76 C. fusus 990.38 1413.33 0 801.24 41.67 2.06
77 C. horridum 288.83 691.21 330.13 436.72 58.33 1.12
78 C. lineatum 1547.49 670.58 206.33 808.13 41.67 2.08
79 C. macroceros 392 196.015 20.63 202.88 33.33 0.52
80 C. paradoxides 660.26 422.98 402.35 495.19 41.67 1.27
81 C. trichoceros 0 897.52 165.06 354.20 25 0.91
82 C. tripos 526.15 464.22 0 330.12 25 0.85
83 C. vulture 0 20.63 0 6.88 8.33 0.02
84 C. breve 0 0 247.6 82.53 8.33 0.21
85 C. karstenii pavillard 0 0 30.95 10.32 8.33 0.02
86 Dinophysis caudata 959.43 2599.77 495.2 1351.47 66.67 3.48
87 D. hastata 0 361.08 0 120.36 16.67 0.31
88 D. fortii 0 350.76 0 116.92 8.33 0.30
89 D. miles 907.85 0 495.18 467.68 33.33 1.20
90 D. sp. 732.47 0 0 244.16 8.33 0.63
91 Gonyaulux sp. 154.75 0 0 51.58 8.33 0.13
92 G. spinifera 361.07 0 0 120.36 8.33 0.31
93 Protoperidinium depressum 402.32 639.62 0 347.32 16.67 0.89
94 P. divergents 546.77 0 0 182.29 8.33 0.47
95 P. sp. 1052.27 784.05 216.65 684.32 33.33 1.76
96 P. oceanicum 206.33 0 0 68.78 8.33 0.18
97 Phalacroma sp. 72.21 0 0 24.07 8.33 0.06
98 Prorocentrum gracile 61.90 0 0 20.63 8.33 0.05
99 Prorocentrum sp. 0 495.17 226.96 240.71 25 0.62
100 Pyrophacus sp. 299.18 350.75 30.95 226.96 25 0.58
101 Pyrocystis sp. 288.86 0 226.96 171.94 25 0.44
102 Tetradinium javanicum 0 987.89 646.18 544.69 50 1.40

provided in Fig. 5. Species-environment correlation for axes 1,

2, 3 and 4 were 0.978,0.980,0.975 and 0.993 respectively. CCA
analysed in a linear model (α = 0.67) showed the influence of
different hydro-biological factors like pH, temperature, DO, TDS,
conductivity, salinity, nitrate, phosphate, ammonium, chlorophyll
a on the distribution and abundance of phytoplankton. Angular
distance and length of the arrows indicated the positive and
negative correlation with the phytoplankton species assemblage.
Phytoplankton distribution and species abundance pattern with
physical and chemical parameters and seasonality demonstrated
that surface water temperature; salinity, pH, ammonium, and
nitrate have a profound influence on species composition in the
dry season (Fig. 5).

3. Discussion

The diversity, distribution, abundance, and composition of

phytoplankton are linked with favourable environmental param-
eters such as pH, temperature, salinity, dissolved oxygen and
nutrients in estuarine and coastal waters (Sridhar et al., 2006;
Upadhyay, 1988; Dwivedi et al., 2006; Rajkumar et al., 2009). Fig. 5. Canonical Correspondence Analysis (CCA) showing triplot distribution
Most of the hydrobiological factors with seasonality were found of phytoplankton species vs environmental variables during the study period.
to be significantly different in the present study (Table 1). These Numeric is denoting specific species as mentioned in Table 3.
differences could be due to seasonal changes in rainfall, salinity,
and temperature. Generally, the influence of salinity, DO, pH and et al., 2013). In the present study, the abundance of phyto-
TDS on the abundance of phytoplankton is well recognized in plankton showed significant correlation with rainfall, ammonium,
different studies (Lassen et al., 2004; Sridhar et al., 2006; Rahman silica, and chlorophyll a.
 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826 9

Table 4
Results of ANOSIM and SIMPER showing the Global R, significance level (P), average dissimilarity
between seasons as well as contribution of major discriminating phytoplankton species among
various seasons.
ANOSIM (Global R = 0.23; P = 0.001)
SIMPER
Season R P Average Major discriminating species Contribution
dissimilarity (%)
(%)
Thalassionema nitzschioides 2.44
Nitzschia sp. 2.27
Ceratium fusus 2.22
Dry vs. Int −0.05 0.5 61.65 Chaetoceors pseudocurvisetus 1.95
Oscillatoria sp. 1.90
Dinophysis caudata 1.89
Rhizosolenia imbricata 1.69
Ceratium carriense 1.69
Thalassionema nitzschioides 2.43
Nitzschia sp. 2.27
Ceratium fusus 2.23

Dry vs. Wet 0.22 0.07 56.90 Chaetoceors pseudocurvisetus 1.95

Oscillatoria sp. 1.90
Dinophysis caudata 1.89
Rhizosolenia imbricata 1.69
Ceratium carriense 1.69
Nitzschia sp. 2.80
Bacillaria paradoxa 2.56
Rhizosolenia clevei 2.52
Int vs. Wet 0.01 0.01 65.17 Tetradinium javanicum 2.45
Ceratium furca 2.19
Ditylum brightwelli 2.14
Thalassionema nitzschioides 2.08

Generally, in the estuarine environment, nutrients are con- Sidik et al., 2008; Costa et al., 2009; Biswas et al., 2010; Canini
sidered to be vital components playing an important role in et al., 2013). A total of 102 species of phytoplankton under 43
the growth, reproduction, and metabolic rates of organisms. Of genera were recorded from this mangrove-dominated river estu-
the dissolved nutrients that possibly influence phytoplankton ary, and an almost similar observation was noticed in Perak river
diversity, ammonium and silica appeared to be of particular im- estuary in Malaysia (Nursuhayati et al., 2013). Meanwhile, the
portance for the estuary. A similar observation regarding the number of species recorded present in study was higher than that
influence of ammonium was also reported in Pichavaram man- of reported in Kuantan, Malaysia (Mohammad-Noor et al., 2012),
grove in India (Perumal et al., 2009). Ammonium is a limiting mangrove estuary in Philippines (Canini et al., 2013), Sundarban
factor in phytoplankton growth (Wu et al., 2011; Dalu et al., mangrove forest, Bangladesh (Aziz et al., 2012) and Kaduviyar
2014). Generally, high concentrations of ammonium into the estuary (Perumal et al., 2009). The similar species composition
aquatic environment can also be contributed by the death and that recorded in the present study were also reported earlier in
subsequent decomposition of phytoplankton and also attributed this region by Boonyapiwat (1983) and Nursuhayati et al. (2013).
to the excretion of ammonia by planktonic organisms (Segar and A total of 43 genera that reported in the present study remained
Hariharan, 1989). Similarly, the concentration of silica also acts as close to 41 genera reported by Sidik et al. (2008) in a Malaysian
a limiting nutrient for diatom growth and change the community estuary in Sepanggar Bay, Sabah.
structure (Tilstone et al., 2003). Thus, a higher concentration of Among the phytoplankton recorded, in general, diatom-
silica in the Sibuti mangrove, probably the cause of the higher dominated in the whole study period with 63 species, which
abundance of diatom (Rahman et al., 2013). Though there was constituted 62% of the total composition. A similar dominance of
revealed no significant correlation of phytoplankton abundance diatom was also reported in Panggol estuary (Chua, 1973); else-
with nitrate and phosphate, however, those nutrients are also where (Kannan and Vasantha, 1992), Pichavaram mangrove estu-
reported as controlling factor of composition and abundance of ary (Perumal et al., 2009) and Southeast coast of India (ThillaiRa-
phytoplankton and even on blooming (Wang et al., 2006). A jasekar et al., 2010). In a similar study, diatom was found 80%
certain amount of nutrients is essential for aquatic organisms like of the total phytoplankton in Matang river estuary (Tanaka and
phytoplankton for their growth and cell development (Harris and Choo, 2000), which is higher than that of present finding. Usually,
Baxter, 1996; Spatharis et al., 2007). Phosphate is a vital compo- diatoms are found dominating in the mangrove waters which
nent for the growth and sustenance of phytoplankton (Verlencar could be due to their capacity of adaptation to widely changing
and Desai, 2004). hydrographical conditions (Rajasegar et al., 2000; Gowda et al.,
Chlorophyll a concentration in water usually expresses the 2001).
biomass of phytoplankton (Lisha et al., 2012). Chlorophyll a Dinoflagellates were found as the second largest group in
demonstrated positive correlation with phytoplankton in the the present study comprising 29 species. Perumal et al. (2009)
present study, which is in agreement with Pichavaram mangrove postulated 16 species of dinoflagellates in Kaduviyar mangrove
estuary, India (Perumal et al., 2009). estuary which revealed lower than that of the present finding.
The phytoplankton community in Sibuti mangrove estuary However, the species composition of dinoflagellates in Sibuti
was found mainly composed in order of Diatom > Dinoflagellate mangrove estuary was found smaller than that of reported by
> Cyanophyta > Chlorophyta. The similar assemblage was also Naqqiuddin et al. (2013) but larger than those recorded by Rajku-
reported in different tropical estuarine systems (Gin et al., 2000; mar et al. (2009) in Pichavaram mangrove waters. Dinoflagellates
10 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826

Table 5
Seasonal succession of different Species/taxa of phytoplankton recorded during the study period at
Sibuti Mangrove Estuary (SME).
Name Average Average % %
abundance similarity contribution cumulative
(cells L−1 ) (%)
Intermediate season (Average similarity: 27.02%)
Coscinodiscus granii 1857 2.88 10.66 10.66
Coscinodiscus centralis 1991.1 2.80 10.37 21.03
Nitzschia sp. 1764.1 2.46 9.12 30.15
Coscinodiscus sp. 1609.4 2.29 8.48 38.63
Ceratium furca 1155.5 1.67 6.19 44.82
Rhizosolenia styliformis 918.17 1.21 4.49 49.31
Rhizosolenia clevei 1176.1 1.14 4.22 53.53
Ditylum brightwelli 1072.9 1.09 4.05 57.59
Ceratium lineatum 1547.5 0.78 2.87 60.46
Rhizosolenia imbricata 660.25 0.64 2.35 62.81
Chaetoceors pseudocurvisetus 1227.7 0.58 2.13 64.95
Rhizosolenia curvata 1093.6 0.56 2.09 67.04
Thalassionema frauenfeldii 959.43 0.56 2.06 69.10
Chaetoceros coarctatus 588.04 0.52 1.93 71.03
Spirogyra sp. 1031.7 0.49 1.85 72.87
Chaetoceros affinis 649.93 0.49 1.82 74.69
Ceratium fusus 990.4 0.49 1.80 76.50
Dinophysis caudata 959.45 0.48 1.76 78.26
Rhizosolenia alata 887.23 0.48 1.76 80.03
Triceratium sp. 969.76 0.45 1.68 81.71
Dinophysis miles 907.86 0.43 1.60 83.31
Hyalodiscus sp. 784.07 0.40 1.48 84.79
Thalassiosira sp. 557.09 0.38 1.39 86.18
Chaetoceros decipiens 618.98 0.38 1.39 87.58
Biddulphia mobiliensis 618.98 0.38 1.39 88.97
Pleursigma normanii 1165.8 0.35 1.31 90.28
Dry season (Average similarity: 26.48%)
Biddulphia mobiliensis 2187.1 3.65 13.81 13.81
Pleursigma normanii 1991.1 2.37 8.97 22.78
Dinophysis caudata 2599.8 1.81 6.82 29.61
Coscinodiscus sp. 1650.7 1.57 5.93 35.53
Odontella sinensis 1475.3 1.44 5.45 40.99
Coscinodiscus granii 1227.7 1.16 4.38 45.37
Coscinodiscus thorii 1176.1 1.12 4.25 49.62
Ceratium carriense 1372.1 1.05 3.97 53.59
Coscinodiscus jonesianus 990.4 0.98 3.70 57.29
Rhizosolenia polydactyla 1011 0.90 3.39 60.69
Ceratium fusus 1413.4 0.87 3.27 63.96
Nitzschia sp. 1661 0.85 3.22 67.19
Ditylum sol 1124.5 0.81 3.05 70.24
Hyalodiscus sp. 773.75 0.71 2.69 72.94
Skeletonema costatum 1083.2 0.69 2.61 75.54
Coscinodiscus centralis 1083.2 0.67 2.55 78.09
Chaetoceors pseudocurvisetus 1465 0.52 1.97 80.06
Thalassionema frauenfeldii 1059.2 0.46 1.74 81.80
Tetradinium javanicum 987.9 0.39 1.49 83.29
Protoperidinium sp. 784.07 0.38 1.42 84.72
Anabaena sp. 742.8 0.37 1.41 86.14
Rhizosolenia clevei 1000.7 0.37 1.38 87.52
Melosira sp. 711.85 0.36 1.37 88.89
Dinophysis hastate 361.08 0.33 1.26 90.16
Wet season (Average similarity: 49.28%)
Pleursigma normanii 1186.4 4.63 9.40 9.40
Thalassionema nitzschioides 1165.8 4.55 9.24 18.64
Hyalodiscus sp. 1021.3 4.09 8.30 26.95
Coscinodiscus sp. 1072.9 3.99 8.09 35.05
Skeletonema costatum 1083.2 3.51 7.12 42.17
Anabaena sp. 753.12 2.94 5.97 48.14
Rhizosolenia alata 794.38 2.84 5.70 53.85
Rhizosolenia polydactyla 773.75 2.70 5.48 59.33
Bacillaria paradoxa 938.81 2.23 4.53 63.87

(continued on next page)

were found dominated by Ceratium, which alone comprised 12 Cyanophyta and Chlorophyta comprised of a very small share
species. Similar dominance of Ceratium in marine and coastal of the total phytoplankton in Sibuti mangrove estuary which re-
vealed almost similar to the finding of Chua (1973) and Rajkumar
water of Malaysia has also been reported by Naqqiuddin et al. et al. (2009) but smaller than that of recorded by Sevindik (2010).
(2013). Species recorded under these two families were mostly observed
 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826 11

Table 5 (continued).
Name Average Average % %
abundance similarity contribution cumulative
(cells L−1 ) (%)
Tetradinium javanicum 646.18 1.99 4.03 67.90
Coscinodiscus centralis 876.91 1.83 3.71 71.61
Coscinodiscus granii 835.65 1.79 3.63 75.25
Biddulphia mobiliensis 577.73 1.44 2.93 78.18
Rhizosolenia imbricata 567.42 1.27 2.57 80.75
Coscinodiscus jonesianus 495.2 1.00 2.04 82.80
Odontella sinensis 371.4 0.81 1.65 84.44
Rhizosolenia curvata 474.57 0.66 1.34 85.77
Oscillatoria sp. 226.97 0.65 1.32 87.09
Navicula sp. 371.4 0.59 1.20 88.29
Spirogyra sp. 299.18 0.53 1.07 89.36
Dinophysis caudata 495.2 0.53 1.07 90.43

either in intermediate or in the wet season, which could be due in Lake Fort Smith (Hoffman, 1952), Pichavaram mangrove es-
to their low salinity tolerance capacity. tuary (Rajkumar et al., 2009) and Perak estuary, Malaysia (Nur-
The overall abundance of phytoplankton in the estuary ranged suhayati et al., 2013), which could be due to dilution caused by
from 5694 to 88 890 cells L−1 , which revealed some extent similar heavy precipitation during that period. Whereas, the dry season
to that of Kaduviyar estuary (Perumal et al., 2009) and Kuantan demonstrated the highest abundance of phytoplankton, which
estuary, Malaysia (Mohammad-Noor et al., 2012) but lower than coincided with the observation of Canini et al. (2013). The more
the findings of Chua (1973), Rajkumar et al. (2009) and Rahman stable physicochemical condition of the estuary during the dry
et al. (2013) elsewhere. However, each estuarine system may
season could be the cause of more species composition and abun-
have a different abiotic environment (Blaber, 1997), governed
dance (ThillaiRajasekar et al., 2005; Prasath et al., 2011). Also, a
by the tidal range, freshwater input, geomorphology and human
wide range of salinity during the dry season enabled more salinity
pressure (McLusky and Elliott, 2004) and those also affect the
species abundance. So a difference in species abundance is not tolerant species to form the community in the estuary.
likely to be the exception. On the contrary, lower abundance of phytoplankton in the wet
The diatom formed a bulk abundance of phytoplankton like- season, in the Sibuti mangrove estuary coincided with the find-
wise its large species composition in the river estuary. Similar ings of the Perak estuary in Malaysia (Nursuhayati et al., 2013), in
dominance in the abundance of diatom was also reported in dif- Lake Fort Smith (Hoffman, 1952) and Aby lagoon system in Ivory
ferent areas on the east coast of Peninsular Malaysia (Boonyapi- coast (Seu-Anoi et al., 2011). During the wet season, the water
wat, 1999; Saleh and Ruslan, 2010). However, the recorded abun- column remains more stratified because of huge precipitation,
dance of diatom in this study revealed lower than that of the high turbidity due to land run-off, low water temperature, low
Qua Iboe Estuary mangrove swamp, Nigeria (Essien et al., 2008) salinity, low pH and cloudy sky, which could be the governing
and the Changjiang Estuary, China (Gao and Song, 2005). The factor for the lower abundance of phytoplankton during the wet
abundance of diatom was largely contributed by some dominant season (Rajkumar et al., 2009). However, during this period some
species viz. Pleurosigma normanii, Coscinodiscus sp., Coscinodiscus freshwater algal forms like Anabaena sp. and Spirogyra sp. were
centralis, Coscinodiscus granii, Nitzschia sp. and Biddulphia mo- observed which could be due to the low salinity caused by heavy
biliensis. Dominant species demonstrated a high frequency of precipitation.
occurrence, which could be due to their wide range of salinity
The overall species diversity index of the study area irrespec-
tolerance and adaptive capacity to changing the environment.
tive of seasons was 3.10, which is comparable with other findings,
Among the dominant species, Coscinodiscus spp. have been re-
ported as common and dominant in several studies (Rajkumar such as Perak estuary, Malaysia (H = 3.4−3.5)(Nursuhayati et al.
et al., 2009 and Mohammad-Noor et al., 2012). Along with nat- 2013). On the contrary, diversity index in the present study was
ural occurring species, some harmful algal bloom (HAB) species found lesser than that of Pichavaram mangrove estuary (3.20-
were also observed in diatom including Coscinodiscus spp., Cer- 5.23) and Palk Bay (3.99 to 5.28). The species diversity index
atium fusus, and Skeletonema costatum though the density of those of plankton community in the estuarine regime can serve as an
species was quite below the bloom formation level (Dickman indicator whether the ecosystem is under the influence of pollu-
et al., 2002). Such harmful algal bloom species were also recorded tion stress or eutrophication (Telesh, 2004) where lower diversity
in the east coast of Sabah by Mohammad-Noor et al. (2012). index stands for pollution stress of the ecosystem. Thus, the
Dinoflagellates have been reported as the second larger group revealed moderate diversity index in the Sibuti estuary confirms
in several studies (Rajkumar et al., 2009; Sevindik, 2010; Canini its healthiness.
et al., 2013). The similar observation was also noticed in the Canonical Correspondence Analysis (CCA) revealed the rela-
present study. Mainly, the dominant species like Dinophysis cau- tionship of phytoplankton abundance with hydrobiological pa-
data, Ceratium fusus, and Ceratium lineatum contributed the major rameters (Fig. 5). In CCA, species plotted closer to the vector,
share to the total abundance of dinoflagellates. These species are possessed stronger relationships with the respective parameters.
mostly marine to brackish and reported as frequent to subdom-
Species located near the origin either do not show a strong
inant in elsewhere (Naqqiuddin et al., 2013). Among the species
relationship to any of the variables or are found at average values
reported, Dinophysis caudata is considered as Diarrhetic Shellfish
of environmental variables. This triplot correspondence analysis
Poisoning Species (DSP) (Naqqiuddin et al., 2013) though in the
present study the abundance was quite small changes in water confirmed the influence of different environmental parameters
quality can give rise to higher abundance towards bloom. on the abundance of phytoplankton. The findings of the present
Likewise, the species composition, the variation of phyto- study exerted an interlinked pattern where phytoplankton being
plankton abundance also followed seasonality. A significant sea- in the centre are facilitated by abiotic parameters viz., pH, tem-
sonal variation in species abundance was observed in Sibuti man- perature, salinity, TDS, DO, rainfall (Fig. 6). Such interactions were
grove estuary where the wet season brought about a lower abun- also reported by Chew et al. (2012), Saifullah et al. (2014), Chua
dance of phytoplankton. The similar observation was also noticed (1973), Rajkumar et al. (2009) and Lohrenz et al. (1988).
12 A.S.M. Saifullah, A.H.M. Kamal, M.H. Idris et al. / Regional Studies in Marine Science 32 (2019) 100826

Fig. 6. Ecological functioning model of SME based on analytical results of Hydrological, biological and chemical variables.

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