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BIODIVERSITAS ISSN: 1412-033X
Volume 21, Number 9, September 2020 E-ISSN: 2085-4722
Pages: 4022-4033 DOI: 10.13057/biodiv/d210913
Distribution of zooplankton community in Toli shad (Tenualosa toli)
habitats, Sarawak, Malaysia
WAN MOHAMAD AIMAN1
, FATIMAH MD YUSOFF3
, AZIZ ARSHAD3
, ABU HENA MUSTAFA KAMAL2,♥
,
JOHAN ISMAIL1
, MOHD HANAFI IDRIS2
, NURUL ULFAH KARIM2
, ABDULLA AL ASIF1
1Department of Animal Science and Fishery, Faculty of Agriculture and Food Sciences, Universiti Putra Malaysia Campus Bintulu. Nyabau Rd, 97008
Bintulu, Sarawak, Malaysia
2Faculty of Fisheries and Food Science, Universiti Malaysia Terengganu. 21030 Kuala Nerus, Terengganu, Malaysia.
Tel./fax.: +60-9-6685001, ♥email: a.hena@umt.edu.my
3Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia. Serdang 43400, Selangor Darul Ehsan, Malaysia
Manuscript received: 25 April 2020. Revision accepted: 10 August 2020.
Abstract. Aiman WM, Yusoff FM, Arshad A, Kamal AHM, Ismail J, Idris MH, Karim NU, Asif AA. 2020. Distribution of zooplankton
community in Toli shad (Tenualosa toli) habitats, Sarawak, Malaysia. Biodiversitas 21: 4022-4033. The river ecosystems of Sarawak has
been identified as important-spawning ground for economically important Toli shad (Tenualosa toli) fisheries. In these river ecosystems,
zooplankton serves as a secondary producer to the different types of fish larvae including Toli shad. The productivity and biomass of
zooplankton are important factors to control the production of higher trophic level organisms like fish larvae and fishes in different stages
including T. toli larvae. In this viewpoint, the composition and abundance of zooplankton were investigated at 5 (five) sampling stations
(considered to be spawning and nursing areas of Toli shad) at Batang Lupar and Batang Sadong estuaries from July 2016 to June 2017. A
total of 29 zooplankton taxa were recorded that belong to 14 major groups comprised of Copepoda (Arthropoda), Crustacean nauplii
(Arthropoda), Fish larvae (Chordata), Mollusca (Mollusca), Luciferidae (Arthropoda), Cnidaria (Cnidaria), Ostracoda (Arthropoda),
Cirripedia (Arthropoda), Polychaete larvae (Annelida), Chaetognatha (Chaetognatha), Appendicularia (Chordata), Amphipoda
(Arthropoda), Echinodermata larvae (Echinodermata) and Cladoceran (Arthropoda). Copepod was dominant group of zooplankton (82.40-
94.41%) at all stations, contributing 477.37-25921.89 ind/m3
and 88.38% of total abundance. The second highest was crustacean larvae
(2.45-9.38%) in all stations, contributing 0-2391.7 ind/m3
and 5.88% of total abundance. Zooplankton abundance was higher at downstream
station 1 (8460.72 ind/m³) followed by station 2 (5479.80 indi/m³), station 3 (4571.95 ind/m³), station 4 (4394.20 ind/m³) and upstream
station 5 (4156.73 ind/m³). Canonical Correspondence Analysis showed that the abundance of copepods was highly influenced by total
turbidity and nitrate in the riverine and estuarine ecosystems. Abundance of zooplankton was relatively higher (9549.31 ind/m³) during the
post-monsoon and lower (3534.56 ind/m³) during the southwest monsoon.
Keywords: Malaysia, Sarawak, Toli shad, Tropical Borneo, zooplankton
INTRODUCTION
The presence of zooplankton is the key indicator of the
healthiness of a water body (Ismail and Adnan 2016). It
also plays a significant ecological role in the food web in
any aquatic ecosystem (Cook et al. 2007). It recycles
micro-macro nutrients including organic matter
transformation (Edwards, 2001) from primary producers to
secondary consumers like fishes (Thirunavukkarasu et al.
2013). High-value commercial fishes mainly Toli shad
(Tenualosa toli) used to migrate turbid and brackish estuary
(Mohsin and Ambak 1996) for spawning and nursing in
Sarawak waters, Malaysia, where zooplankton community
plays a vibrant role for nourishment to different
commercial species up to juvenile from larvae including
Toli shad (Tumiran et al. 2011; Rahim et al. 2014). Studies
showed that the seasonal distribution and abundance of
zooplankton represented in dissimilar patterns throughout
the season in a year elsewhere (Srichandan et al. 2013;
Buttay et al. 2015; Marcolin et al. 2015; Abu Hena et al.
2016; Abdullah et al. 2018).
Estuaries are usually non-isolated and highly tidal
region with the change of all physicochemical parameters
that influence the planktonic food sources for fishes found
in tropical estuarine ecosystems (Harrison 2004; Hossain et
al. 2012; Saifullah et al. 2014; Paturej et al. 2017).
Previously, Chew and Chong (2010); Rezai et al. (2011);
Lee (2012); Zaleha et al. (2013); Zulikha et al. (201)3;
Kassim et al. ( 2015); Matias-Peralta and Yusoff (2015);
Musa and Singh (2015); Azmi et al. (2016); Fatema and
Omar (2016); Saidin (2016); Yong et al. (2016);
Kamaruzaman et al. (2018) had documented the seasonal
distribution of zooplankton from both the riverine and
estuarine water of Malaysia. Although several studies have
been undertaken in Peninsular Malaysia, a few zooplankton
studies dealt in the estuarine and riverine habitats in east
Malaysia (Jivaluk 1999; Johan et al. 2013; Sinev and
Yusoff 2015; Sinev and Yusoff 2018). Furthermore, there
are no previous studies revealed on the temporal population
structure of zooplankton in Sarawak riverine and estuarine
waters, which is very well known for the historical T. toli
shad spawning (Rahim et al. 2014) and nursery ground.
Considering an important breeding area of a high valued
AIMAN et al. – Zooplankton community structure of a tropical estuary 4023
commercial species, this study was undertaken to assess the
zooplankton availability, abundance and ecological
interactions in one of the Toli shad habitats, namely Batang
Lupar and Batang Sadong estuaries, Sarawak. The findings
of this study help to know the zooplankton community and
distribution in these estuarine ecosystems which would
help to understand the spatial and temporal distribution of
zooplankton of Toli shad breeding ground along with their
ecosystem functions. The findings of this study eventually
are usual for habitat conservation and sustainable
management of this important fishery resources in Sarawak
waters, Malaysia.
MATERIALS AND METHODS
The study was conducted in the south-western part of
Sarawak, the Batang Lupar and Batang Sadong estuarine
complex. Five (5) sampling stations (Figure 1) were
selected along the Batang Lupar and Batang Sadong
estuaries encompassing the importance for the spawning
ground of Tenualosa toli and all sampling locations
relocated with a differentially corrected Global Positioning
System (GPS) receiver (Model Garmin, GPS 76, SN
80308437, Olathe USA). The field samples collected from
surface water from the selected stations monthly from July
2016 to June 2017.
Collection and identification of zooplankton
Zooplankton was collected monthly for 12 consecutive
months (a year) from surface waters (<1 m depth) of the
selected area using a zooplankton net of 150 μm mesh size
with 0.35 m mouth diameter (Sameoto et al. 2000). All
samples were done at three replication. The flow meter was
mounted at the center of the mouth of net to measure the
rate or quantity of water passed into the net (Smith et al.
1968) and the net was towed horizontally at the surface for
5 minutes following Wiebe et al. (2014). Collected samples
were put into a 250 ml plastic bottle and preserved by
neutralized 5% formalin. All samples were brought to the
Aquatic Laboratory of Universiti Putra Malaysia Bintulu
Sarawak Campus for further analysis and identified
following Chihara and Murano (1997).
The major taxonomic groups of zooplankton were
determined under the microscope (Leica, Model: Z45V)
using a counting chamber. Samples were analyzed for the
determination of zooplankton diversity and abundance
using standard works of Kasthuriranagn (1963).
Zooplankton samples were fractioned before analysis using
Motodo Plankton Splitter. Zooplankton abundance was
calculated based on total area hauled by the plankton net
and volume of water filtered was measured by the
following equations:
Figure 1. Map of the study area showing sampling location (Stations 1 to 5) in Batang Lupar and Batang Sadong estuaries, Sarawak,
Malaysia
BIODIVERSITAS 21 (9): 4022-4033, September 2020
4024
The volume of water filtered through the zooplankton
net was calculated by the equation of,
The volume of filtered water (m3
)
Where, r: radius of the mouth of the plankton net (m),
and pie: 3.142, d: Length of the water column traversed by
the net. Total hauling area (d): 1 meter *flow meter reading
(5 rotor count is equal to 1 m)/flow meter standard.
Then the abundance of zooplankton was calculated by
the following equation:
The abundance of zooplankton (individual/m³) =
Collection of ecological samples and analysis of
ecological parameters
In-situ parameters of surface water were measured in all
stations, including temperature, salinity, pH, dissolved
oxygen, conductivity, and turbidity by using multi-
parameter (Model Hydro-lab, WQC-24). Water samples
were collected randomly from the water surface of river
estuary from three sampling areas (replications) of a station
by following Environmental Protection Agency guidelines,
EPA (2008). In the laboratory, water nutrients including
total suspended solids (TSS), chlorophyll a, ammonia
(NH3), nitrate (NO3), phosphate (PO4) and Silica (SiO2)
analyzed. Water nutrients were analyzed by APHA
standard methods (2005) in the laboratory. The data of
zooplankton diversity and other ecological factors were
transformed and performed the normality test. normality
Then a two-way ANOVA was performed on various
abiotic factors and zooplankton groups to find out the
variations in physicochemical parameters, population
density, species diversity, and diversity index. The
Shannon-Wiener index (H´) was used to summarize the
information on the relative abundance of zooplankton
found within the study area. The relationship between
physicochemical parameters and population abundance of
zooplankton was analyzed using the Canonical
Correspondence Analysis (CCA). Zooplankton abundance
according to stations were classified using cluster analysis,
and similarity (ANOSIM) by using MVPS 3.1 and PAST
(3.0) version software.
RESULTS AND DISCUSSION
Zooplankton diversity
A total of 29 zooplankton species was recorded in the
present study which belongs to 14 major groups of
zooplankton (Table 1) represented by Copepoda,
Crustacean nauplii, Fish larvae, Mollusca, Luciferidae,
Cnidaria, Ostracoda, Cirripedia, Polychaete larvae,
Chaetognatha, Appendicularia, Amphipoda, Echinodermata
larvae and Cladocera.
Table 1. Major groups of zooplankton at toli shad breeding ground area, in Sarawak, Malaysia
Phylum Class Order Family Genus
Arthropoda Hexanauplia Calanoida Paracalanidae Acrocalanus spp.
Paracalanus spp.
Bestiolina spp.
Centropagidae Centropages spp.
Acartiidae Acartia spp.
Pontellidae Labidocera spp.
Calanidae Canthocalanus spp.
Cosmocalanus spp.
Cyclopoida Oithonidae Oithona spp.
Corycaeidae Corycaeus spp.
Harpacticoida Tachidiidae Euterpina spp.
Cirripedia larvae
Malacostraca Amphipoda Gammaridea Amphipod spp.
Decapoda Sergestidae Acetes spp.
Isopoda Isopod
Crustacea Shrimp larvae.
Zoea
Nauplii
Ostracoda Ostracod
Branchiopoda Cladocera
Mollusca Bivalvia Bivalve larvae
Gastropoda Gastropod larvae
Chordata Actinopterygii Stomiiformes Stomiidae Lucifer
Appendicularia Copelata Oikopleuridae Oikopleura
Fish larvae and Fish egg
Chaetognatha Sagittoidea Aphragmophora Sagittidae Sagitta spp.
Annelida Polychaeta Polychaete larvae
Cnidaria Cnidaria larvae
Echinodermata Ophiuroidea Echinoderm larvae
Nematoda Nematodes
AIMAN et al. – Zooplankton community structure of a tropical estuary 4025
Percentage of zooplankton group from Tenualosa toli
breeding area
The present study reported that copepods were the
major group (88.38%) of species during the whole study
period, and non-copepods comprised 11.62% in the total
species counted. Non-copepod comprised with Crustaceans
larvae (5.88%), Chaetognatha (2.32%), Mollusca (1.95%),
Polychaeta (0.88%), Cnidaria (0.19%), Fish larvae (0.13%)
and others (0.27%) groups from this Batang Lupar river
estuary (Figure 2).
Zooplankton abundance
The total population densities of zooplankton ranged
from 447.5 to 27812.9 ind/m³ representing from five
stations (Figure 3), and the dominant group, copepod
contributed about 477.37-25921.89 ind/m3
. Zooplankton
abundance in station 1 was higher (8460.72 ind/m³)
followed by station 2 (5479.80 ind/m³), station 3 (4571.95
ind/m³), station 4 (4394.2 ind/m³) and station 5 (4156.73
ind/m³) (Figure 4). The highest total means zooplankton
abundance (10070.39 ind/m³) was recorded in December
2016 while the lowest abundance (1461.47 ind/m³) was
observed in July 2016 (Table 2).
The abundance and distribution of zooplankton at all
stations showed that copepod was the dominant group in
terms of composition (Figure 5). Copepod showed 86.05%,
90.57%, 82.40%, 90.82% and 94.41% in total zooplankton
population in stations 1, 2, 3, 4 and 5, respectively. Second
important group was Crustacean nauplii (2.45% to 9.38%)
followed by Chaetognatha (0.30% to 6.64%) and Mollusca
(0.12% to 3.87%).
Ecological parameter
Water salinity and conductivity were significantly
different (p<0.05) in all stations; while, these values were
found higher at stations 1, 2, and 3 but lower at stations 4
and 5 (Table 3). Salinity (16.48 to 46.97 PSU) and
conductivity (24.66 to 57.52 S/m) were the higher at
stations 1, 2, and 3 in July, August, September, April, May,
and June. Turbidity and total suspended solids showed
almost similar trends but, not significantly (p≥0.05)
different. The surface water temperature at all stations was
at the range of 26.0ºC to 26.48ºC (north-west monsoon)
from January to April, while in July to December recorded
in higher trend from 28ᵒC to 31.39ᵒC (Figure 6). The
temperature was not significantly different p≥0.05 among
the station studied (Table 3). The highest water temperature
was recorded (31.39ºC) in August at station 3 and the
lowest (21.95ºC) in June at station 5.
Figure 2. Percentage of zooplankton group from toli shad
(Tenualosa toli) breeding ground area during the study period in
Sarawak, Malaysia
Table 2. Summary result of two-way ANOVA and Tukey HSD tests on various zooplankton groups (mean (ind/m³)±SE)
Zooplankton Station 1 Station 2 Station 3 Station 4 Station 5
Copepoda 7301.84±2075.13a
4277.8±1265.4a
3854.4±605.9a
3955.6±908.6a
4197.8±1152.7a
ns
Crustacean nauplii 618.15±228.22a
230.93±81.2a
438.95±185.7a
171.83±107.4a
108.95±41.5a
ns
Fish larvae 6.47±2.92a
13.53±5.27a
3.85±1.25a
6.32±2.08a
4.59±2.36a
ns
Mollusca 328.89±259.83a
33.76±11.23a
5.43±2.19a
41.26±15.07a
111.13±83.2a
ns
Luciferidea 1.00±0.66a
1.60±1.25a
2.31±1.79a
0.00a
0.00a
ns
Cnidaria 8.36±8.05a
25.65±18.31a
2.67±1.55a
12.34±6.75a
1.18±0.69a
ns
Ostracoda 11.12±10.89a
2.32±1.57a
2.80±2.58a
1.60±1.6a
0.00 a
ns
Cirripedea 10.59±9.13a
0.18±0.18a
0.46±0.46a
1.57±1.34a
2.14±1.21a
ns
Polychaeta 79.66±69.64a
47.90±43.94a
53.62±50.58a
46.82±33.14a
5.80±3.81a
ns
Chaetognatha 101.31±35.61ab
81.32±34.91ab
310.51±102.3a
113.60±71.46ab
13.28±5.66b
**
Appendicularidae 16.98±10.95a
5.66±2.57a
2.53±0.98a
2.04±1.64a
0.19±0.19a
ns
Amphipoda 1.35±0.63a
1.10±1.1a
0.16±0.16a
2.57±2.41a
1.23±0.66a
ns
Echinodermata 0.40±0.0 0a
1.28±1.28a
0.00a
0.00a
0.00 a
ns
Cladocerans 0.00a
0.12±0.12a
0.00a
0.00a
0.00 a
ns
Note: *Correlation is significant at 0.05 level (2-tailed). **Correlation is significant at 0.01 level (2-tailed)
BIODIVERSITAS 21 (9): 4022-4033, September 2020
4026
Water pH was significantly different p<0.01 in all
stations. Riverine and estuarine water were alkaline (7.0 to
8.25) at all stations in July, August and September, while
from October to June it was slightly acidic (stations 1 to 3)
to alkaline (stations 4 and 5), and ranged from 6.75 to 7.5.
Dissolved oxygen (DO) was significantly different
(p<0.05), and found higher in May and June at stations 1 to
3 (5.27 to 10.6 mg/l) and lower in other months in other
stations with the range of 3.0 to 6.25 mg/l. The maximum
mean value of total suspended solids was found at station 1
in July (0.83 mg/l), while the lowest value at station 2 in
November (0.06 mg/l), but not significantly different at all
stations. Chlorophyll a ranged from 0.001 to 0.07 mg/l)
during the study period. Water nutrients (ammonium,
nitrate, phosphate), total suspended solids, chlorophyll a,
and silica showed a non-significant trend (p≥0.05) (Table
3) in all stations (Figure 7).
Ecological indices
The richness index (1.07 to 1.54) was higher at station 2
where 13 zooplankton groups and lowers at station 5 which
comprised nine zooplankton groups. Both the Shannon and
evenness indices were the highest at station 3 and the
lowest at station 5 which Shannon indices were within the
range of 0.28 to 0.64 and evenness indices were within
0.12 to 0.26 (Figure 8).
ANOSIM analysis of zooplankton population abundance
The similarity of zooplankton abundance among all
stations based on the number of zooplankton found per m3
data (permutation: 9999) revealed that there were no
significant differences (p< 0.30) among stations. The study
also revealed that some stations that were located in a
similar habitat shared high similarity in abundance among
the stations. The study revealed, station 1 was very similar
with station 2 (similarity index: 0.18), and very dissimilar
with station 3 (similarity index: 0.32); station 2 was very
similar with station 3 (similarity index: 0.11), and very
dissimilar with station 4 (similarity index: 0.43); station 3
was very similar with station 2 (similarity index: 0.11), and
very dissimilar with station 5 (similarity index: 0.61);
station 4 was very similar with station 1 (similarity index:
0.25), and very dissimilar with station 3 (similarity index:
0.62); station 5 was very similar with station 2 (similarity
index: 0.29), and very dissimilar with station 3 (similarity
index: 0.67) (Table 4).
Table 3. Summary results of two-way ANOVA and Tukey HSD tests on various abiotic factors (mean±SE)
Parameter
Station
p
Station 1 Station 2 Station 3 Station 4 Station 5
Salinity (psu) 22.265±2.24ᵃᵇ 26.85±2.56ᵃ 16.58±1.28ᵇ 8.77±1.21ᶜ 5.66±0.95ᶜ *
Conductivity (S/m) 34.993±3.22ab
41.94±3.39a
27.01±1.88b
15.01±2.03c
9.89±1.55c
*
Temperature (⁰C) 27.65±0.71a
27.61±0.73a
28.61±0.74a
28.36±0.82a
27.812±0.8a
ns
pH 7.363±0.13ᵃᵇ 7.63±0.12a
7.36±0.13ab
6.996±0.17b
7.02±0.16b
**
Turbidity (NTU) 181.75±38.60a
186.57±17.80a
135.98±14.8a
204.7±32.39a
196.27±22.0a
ns
DO (mg/L) 5.011±0.50ab
6.17±0.46a
4.99±0.27ab
4.21±0.21b
4.42±0.25b
*
TSS (mg/L) 0.728±0.18a
1.14±0.52a
0.58±0.15a
0.42±0.15a
0.699±0.2a
ns
Chlorophyll a (mg/L) 0.016±0.01a
0.01±0.003a
0.009±0.003a
0.01±0.003a
0.006±0.002a
ns
NH3 (mg/L) 0.0675±0.01a
0.062±0.008a
0.057±0.006a
0.061±0.007a
0.053±0.006a
ns
NO₃-N(mg/L) 0.018±0.002a
0.013±0.002a
0.012±0.002a
0.014±0.002a
0.012±0.002a
ns
PO4-P(mg/L) 0.023±0.008a
0.025±0.007a
0.025±0.006a
0.021±0.005a
0.023±0.005a
ns
SiO (mg/L) 10.78±0.81a
11.132±0.47a
10.968±0.36a
10.65±0.90a
10.397±0.76a
ns
Note: *Correlation is significant at 0.05 level (2-tailed). **Correlation is significant at 0.01 level (2-tailed).
Figure 3. The monthly zooplankton abundance (ind/m³) at Batang Lupar and Batang Sadong (Sarawak, Malaysia) estuarine complex
during the study period
AIMAN et al. – Zooplankton community structure of a tropical estuary 4027
Figure 4. The monthly average abundance of total zooplankton from Batang Lupar and Batang Sadong estuaries, Sarawak, Malaysia
during the study period
Figure 5. Percentage of the zooplankton group from July 2016 until June 2017 in the study areas (ST1-ST5)
BIODIVERSITAS 21 (9): 4022-4033, September 2020
4028
Figure 6. The monthly water quality parameter (in-situ ecological parameter) in Batang Lupar and Batang Sadong estuaries, Sarawak,
Malaysia during the study period
Inter-station cluster analysis
Cluster analysis of zooplankton abundance in all 5
stations revealed a clear inter-stational grouping. The
dendrogram presented the zooplankton density in total
number of stations (5) were generally classified into 2
groups at the similarity level of 0.90 based on the
difference of stations (Figure 9). Station 1 was clearly
separated from another cluster comprised of Stations 2-5.
Canonical correspondence analysis (CCA)
The first canonical axis accounted for 44.65% and the
second axis accounted for 25.17% of the variance in the
zooplankton abundance. Thus the first two axes
cumulatively explain 69.82% of the variance. The third
canonical axis accounted for 21.42% and altogether the
value represents 91.24%. CCA model confirmed that key
abiotic factors notably Turbidity and nitrate (NO3-N) were
highly correlated with individual groups of zooplankton
abundance. Here, ecological parameters such as Turbidity
(eigenvalue: 0.044) and nitrate (eigenvalue: 0.025) were
highly correlated among all other parameters (Figure 10).
Zooplankton groups Cirripedia larvae, mollusks,
amphipods, were found to be closely associated with
turbidity content of water (Figure 10).
AIMAN et al. – Zooplankton community structure of a tropical estuary 4029
Figure 7. The monthly water quality parameters in Batang Lupar and Batang Sadong estuaries, Sarawak, Malaysia during the study
period
Figure 8. Diversity, evenness and richness index of zooplankton at Batang Lupar and Batang Sadong estuaries, Sarawak, Malaysia
BIODIVERSITAS 21 (9): 4022-4033, September 2020
4030
Table 4. The similarity of zooplankton population abundance analyzed by one-way ANOSIM (PAST-3.25) during study periods for 5
stations
S1 S2 S3 S4 S5
S1 0.176 0.326 0.251 0.298
S2 0.175 0.112 0.433 0.291
S3 0.326 0.112 0.617 0.671
S4 0.251 0.431 0.617 0.575
S5 0.298 0.291 0.671 0.575
Figure 9. Dendrogram based on Bray-Curtis similarity between of zooplankton density in different stations in the study area
Figure 10. Canonical correspondence analysis (CCA) ordination depicting relationships among abundances of zooplankton and
environmental variables
AIMAN et al. – Zooplankton community structure of a tropical estuary 4031
Table 5. Comparison of zooplankton abundance with other studies in Malaysia
Habitat Zooplankton Mesh size Reference
Marudu Bay estuaries 1243 to 1553 ind/m3
20 μm Tan and Ransangan (2017)
Lukut estuary, Negeri Sembilan 104300 ind/m3
150 μm Musa and Singh (2015)
Merbok estuary Kedah 361×103
ind/m3
150 μm Fatema and Omar (2016)
Seagrass meadow Johor, Malaysia 17.0 x104
ind/m3
100 μm Matias-Peralta and Yusoff (2015)
Seagrass bed, Merambong shoal 3030.16 to 4006.5 ind/m³ 140 μm Azmi et al. (2016)
Mangrove estuary, Malaysia 12330 - 20311 ind/m3
180 μm Chew and Chong (2011)
Coast of Klang Strait, Malaysia 30951-55756 ind/m3
180-363 μm Chew and Chong (2016)
Borneo coastal waters 232 to 251 ind/m3
0.03 mm Jivaluk (1999)
Seagrass bed, Pulau Tinggi, Johor 1245 ind/m3
100 μm Shuaib et al. (2019)
Straits of Malacca 9202 ind/m3
140 μm Rezai et al. (2011)
Batang Lupar and Batang Sadong estuary, Sarawak 447.5 to 27812.9 ind/m³ 150 μm Present study
Discussion
The research focused on the studies of zooplankton
recently due to its functions in the aquatic ecosystems as
live food and a contributor to the secondary consumers of
the riverine ecosystem. Zooplankton also plays a key
environmental indicator in any aquatic ecosystem as well
as works an important role in the aquatic food chain. A
total of 29 spp. with 14 major groups of zooplankton was
recorded in the present study, which is a moderate number
of species compared to other studies; that is lower than the
value recorded (91 spp.) by Chew et al. (2015) in coastal
estuaries, Abu Hena et al. (2016) in mangrove estuary (33
sp.) and Tinggi and Sibu Islands (129 sp.) Malaysia
(Metillo et al. 2018), and higher than the value of Straits of
Johor (Kassim et al. 2015) and Sungai Lukut (Musa and
Singh 2015).
A comparison of the zooplankton number and
abundance of the present study with other studies is
presented in Table 5. The range of total abundance of
zooplankton was found from 447.5 to 27812.9 ind/m³
representing from 5 stations, which is coincided with the
findings from some coastal and estuarine waters (Table 5).
The abundance of zooplankton recorded from these 2
estuarine habitats was higher than that of (232±125 ind/m3
)
reported by Jivaluk (1999) in Sabah, Sarawak and Brunei
Darussalam waters and comparable to that of recorded in
Matang mangroves, Marudu Bay estuaries and Straits of
Malacca (Table 5). Generally, different estuarine and coast
have a different environmental setting (Blaber 1997) due to
the different tidal range, freshwater input, geomorphology,
and human pressure (McLusky and Elliott 2004), which
can also be driving force in a variation of the abundance of
zooplankton in a different regime.
Studies revealed that crustaceans, especially copepods
form a major portion of the zooplankton community in
most of the estuarine regime (Abu Hena et al. 2016). In the
present study, copepods were found occupying 88.38% of
the total zooplankton, which is lower than that of 94.7%
reported by Zulikha et al. (2013) in Perak river, Malaysia.
In the context of the number of species, the present finding
revealed lower than that of 49 species identified from the
Bintulu coast (Johan et al. 2013) and 48 species in Sangga
estuary, Malaysia (Chew and Chong 2011). It is assumed
that different factors such as sampling apparatus, duration,
and area of coverage could attribute to the different
findings regarding species composition (Johan et al. 2013).
Calanoida constituted a large number of species of copepod
in the present study, which coincided, with the findings of
Johan et al. (2012) probably due to their continuous
breeding behavior, quick larval development and the
adaptation to the widely changing environment in the
estuary (Perumal et al. 2009).
Copepod contributes about 477.37-25921.89 ind/m3
,
and 88.38% of total zooplankton followed by crustacean
larvae 5.88%, Chaetognatha 2.32%, Mollusca 1.95%,
Polychaeta 0.85% and others (0.59%). Zooplankton
abundance was higher (8460.72 ind/m³) in station 1
followed by station 2 (5479.80 ind/m³), station 3 (4571.95
ind/m³), station 4 (4394.2 ind/m³) and station 5 (4156.73
ind/m³). It is probably due to higher nutrient input in station
1 from adjacent mangrove ecosystems as noticed by other
studies elsewhere (Abu Hena et al. 2016). The highest total
means zooplankton abundance (10070.39 ind/m³) was
recorded in December 2016 while the lowest abundance
(1461.47 ind/m³) was observed in July 2016. The higher
abundance of zooplankton in December could be directed
by nutrient supply due to higher precipitation in this area,
which provides a favorable condition for zooplankton
development (Abu Hena et al. 2016). This finding is
similar to the studies of Yoshida et al. (2012); Chew et al.
(2015); Kassim et al. (2015) and Tan and Ransangan
(2017) in other tropical and sub-tropical coasts.
Species richness index (1.07 to 1.54) was higher at
station 2 (1.54) which referred to the higher number species
that was found in the downstream area, and populated by a
diverse salinity tolerant species found in the mouth of the
estuary. In the upstream area (station 5), a lower richness
index (1.07) was recorded and these areas were dominated
by freshwater species. The Shannon index was higher at
station 3 (0.64) and lower at station 5 (0.27) while the
Evenness index was 0.25 and 0.12 respectively. These
indices showed that the species homogeneity of the
downstream area stations (station 3) was higher because
this station represented the end-point of downstream areas
and the start-point of upstream areas. Station 5 (upstream)
showed lower homogeneity of species; zooplankton species
assemblage of these areas was very scattered. These are
similar to the findings of Abu Hena et al. (2016) and Ismail
BIODIVERSITAS 21 (9): 4022-4033, September 2020
4032
and Zaidin (2015). The present study also revealed that the
zooplankton composition was similar between some
stations and these stations were considered sharing a
similar habitat (Table 4). A similar observation was also
found by Favier and Winkler (2014) at St Lawrence
estuarine transition zone, Chen and Liu (2015) in the
Yellow Sea and the East China Sea and Bhat et al. (2014)
at tropical wetland India.
Cluster analysis of zooplankton abundance in all five
stations revealed a clear inter-stational grouping. The
dendrogram presented the zooplankton abundance in the
total number of stations (5) were generally classified into 2
groups at the similarity level of 0.90 based on the
difference of stations. The cluster analysis of the present
study was very relevant with the study of Johan et al.
(2012) at Perai river estuary, Penang, Malaysia, and Razak
et al. (2016) at tropical mangrove estuary in the Straits of
Malacca, Malaysia.
Based on CCA, there was no similarity between
ecological and zooplankton abundance with the present
study. However, Metillo et al. (2018) showed the same sort
of CCA elsewhere. The present study found that copepod
was the dominant group in the abundance and composition
of zooplankton could probably due to good environment
support because these species are very useful for coastal
and estuarine fishery resources in this estuarine
environment and associated with water turbidity and
nitrate.
The rivers of Sarawak harbors diverse groups of
zooplankton and could have significant contributions on
the breeding ground for different fish species. Different
ecological parameters were influenced the zooplankton
abundance, diversity, and distribution. The zooplankton
population in the Tenualosa toli habitat exhibited some
degree of population diversity, stable uniformity, and
evenly distributed. Zooplankton population on these
estuarine ecosystems can be used as an indicator of a
healthy aquatic ecosystem. Further study of influences on
zooplankton composition and abundance with the
ecological association on any other fish species, which is
available in these estuarine habitats, is highly
recommended.
ACKNOWLEDGEMENTS
The author is gratefully acknowledgments to TRGS
(TRGS/1/2015/UPM/01/13/3) by the Ministry of Higher
Education, Malaysia for providing financial assistance to
carry out the present research work and Department of
Agriculture, Sarawak for support for sampling activity
during the study period.
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Distribution of zooplankton community in Toli shad (Tenualosa toli) habitats, Sarawak, Malaysia

  • 1. BIODIVERSITAS ISSN: 1412-033X Volume 21, Number 9, September 2020 E-ISSN: 2085-4722 Pages: 4022-4033 DOI: 10.13057/biodiv/d210913 Distribution of zooplankton community in Toli shad (Tenualosa toli) habitats, Sarawak, Malaysia WAN MOHAMAD AIMAN1 , FATIMAH MD YUSOFF3 , AZIZ ARSHAD3 , ABU HENA MUSTAFA KAMAL2,♥ , JOHAN ISMAIL1 , MOHD HANAFI IDRIS2 , NURUL ULFAH KARIM2 , ABDULLA AL ASIF1 1Department of Animal Science and Fishery, Faculty of Agriculture and Food Sciences, Universiti Putra Malaysia Campus Bintulu. Nyabau Rd, 97008 Bintulu, Sarawak, Malaysia 2Faculty of Fisheries and Food Science, Universiti Malaysia Terengganu. 21030 Kuala Nerus, Terengganu, Malaysia. Tel./fax.: +60-9-6685001, ♥email: a.hena@umt.edu.my 3Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia. Serdang 43400, Selangor Darul Ehsan, Malaysia Manuscript received: 25 April 2020. Revision accepted: 10 August 2020. Abstract. Aiman WM, Yusoff FM, Arshad A, Kamal AHM, Ismail J, Idris MH, Karim NU, Asif AA. 2020. Distribution of zooplankton community in Toli shad (Tenualosa toli) habitats, Sarawak, Malaysia. Biodiversitas 21: 4022-4033. The river ecosystems of Sarawak has been identified as important-spawning ground for economically important Toli shad (Tenualosa toli) fisheries. In these river ecosystems, zooplankton serves as a secondary producer to the different types of fish larvae including Toli shad. The productivity and biomass of zooplankton are important factors to control the production of higher trophic level organisms like fish larvae and fishes in different stages including T. toli larvae. In this viewpoint, the composition and abundance of zooplankton were investigated at 5 (five) sampling stations (considered to be spawning and nursing areas of Toli shad) at Batang Lupar and Batang Sadong estuaries from July 2016 to June 2017. A total of 29 zooplankton taxa were recorded that belong to 14 major groups comprised of Copepoda (Arthropoda), Crustacean nauplii (Arthropoda), Fish larvae (Chordata), Mollusca (Mollusca), Luciferidae (Arthropoda), Cnidaria (Cnidaria), Ostracoda (Arthropoda), Cirripedia (Arthropoda), Polychaete larvae (Annelida), Chaetognatha (Chaetognatha), Appendicularia (Chordata), Amphipoda (Arthropoda), Echinodermata larvae (Echinodermata) and Cladoceran (Arthropoda). Copepod was dominant group of zooplankton (82.40- 94.41%) at all stations, contributing 477.37-25921.89 ind/m3 and 88.38% of total abundance. The second highest was crustacean larvae (2.45-9.38%) in all stations, contributing 0-2391.7 ind/m3 and 5.88% of total abundance. Zooplankton abundance was higher at downstream station 1 (8460.72 ind/m³) followed by station 2 (5479.80 indi/m³), station 3 (4571.95 ind/m³), station 4 (4394.20 ind/m³) and upstream station 5 (4156.73 ind/m³). Canonical Correspondence Analysis showed that the abundance of copepods was highly influenced by total turbidity and nitrate in the riverine and estuarine ecosystems. Abundance of zooplankton was relatively higher (9549.31 ind/m³) during the post-monsoon and lower (3534.56 ind/m³) during the southwest monsoon. Keywords: Malaysia, Sarawak, Toli shad, Tropical Borneo, zooplankton INTRODUCTION The presence of zooplankton is the key indicator of the healthiness of a water body (Ismail and Adnan 2016). It also plays a significant ecological role in the food web in any aquatic ecosystem (Cook et al. 2007). It recycles micro-macro nutrients including organic matter transformation (Edwards, 2001) from primary producers to secondary consumers like fishes (Thirunavukkarasu et al. 2013). High-value commercial fishes mainly Toli shad (Tenualosa toli) used to migrate turbid and brackish estuary (Mohsin and Ambak 1996) for spawning and nursing in Sarawak waters, Malaysia, where zooplankton community plays a vibrant role for nourishment to different commercial species up to juvenile from larvae including Toli shad (Tumiran et al. 2011; Rahim et al. 2014). Studies showed that the seasonal distribution and abundance of zooplankton represented in dissimilar patterns throughout the season in a year elsewhere (Srichandan et al. 2013; Buttay et al. 2015; Marcolin et al. 2015; Abu Hena et al. 2016; Abdullah et al. 2018). Estuaries are usually non-isolated and highly tidal region with the change of all physicochemical parameters that influence the planktonic food sources for fishes found in tropical estuarine ecosystems (Harrison 2004; Hossain et al. 2012; Saifullah et al. 2014; Paturej et al. 2017). Previously, Chew and Chong (2010); Rezai et al. (2011); Lee (2012); Zaleha et al. (2013); Zulikha et al. (201)3; Kassim et al. ( 2015); Matias-Peralta and Yusoff (2015); Musa and Singh (2015); Azmi et al. (2016); Fatema and Omar (2016); Saidin (2016); Yong et al. (2016); Kamaruzaman et al. (2018) had documented the seasonal distribution of zooplankton from both the riverine and estuarine water of Malaysia. Although several studies have been undertaken in Peninsular Malaysia, a few zooplankton studies dealt in the estuarine and riverine habitats in east Malaysia (Jivaluk 1999; Johan et al. 2013; Sinev and Yusoff 2015; Sinev and Yusoff 2018). Furthermore, there are no previous studies revealed on the temporal population structure of zooplankton in Sarawak riverine and estuarine waters, which is very well known for the historical T. toli shad spawning (Rahim et al. 2014) and nursery ground. Considering an important breeding area of a high valued
  • 2. AIMAN et al. – Zooplankton community structure of a tropical estuary 4023 commercial species, this study was undertaken to assess the zooplankton availability, abundance and ecological interactions in one of the Toli shad habitats, namely Batang Lupar and Batang Sadong estuaries, Sarawak. The findings of this study help to know the zooplankton community and distribution in these estuarine ecosystems which would help to understand the spatial and temporal distribution of zooplankton of Toli shad breeding ground along with their ecosystem functions. The findings of this study eventually are usual for habitat conservation and sustainable management of this important fishery resources in Sarawak waters, Malaysia. MATERIALS AND METHODS The study was conducted in the south-western part of Sarawak, the Batang Lupar and Batang Sadong estuarine complex. Five (5) sampling stations (Figure 1) were selected along the Batang Lupar and Batang Sadong estuaries encompassing the importance for the spawning ground of Tenualosa toli and all sampling locations relocated with a differentially corrected Global Positioning System (GPS) receiver (Model Garmin, GPS 76, SN 80308437, Olathe USA). The field samples collected from surface water from the selected stations monthly from July 2016 to June 2017. Collection and identification of zooplankton Zooplankton was collected monthly for 12 consecutive months (a year) from surface waters (<1 m depth) of the selected area using a zooplankton net of 150 μm mesh size with 0.35 m mouth diameter (Sameoto et al. 2000). All samples were done at three replication. The flow meter was mounted at the center of the mouth of net to measure the rate or quantity of water passed into the net (Smith et al. 1968) and the net was towed horizontally at the surface for 5 minutes following Wiebe et al. (2014). Collected samples were put into a 250 ml plastic bottle and preserved by neutralized 5% formalin. All samples were brought to the Aquatic Laboratory of Universiti Putra Malaysia Bintulu Sarawak Campus for further analysis and identified following Chihara and Murano (1997). The major taxonomic groups of zooplankton were determined under the microscope (Leica, Model: Z45V) using a counting chamber. Samples were analyzed for the determination of zooplankton diversity and abundance using standard works of Kasthuriranagn (1963). Zooplankton samples were fractioned before analysis using Motodo Plankton Splitter. Zooplankton abundance was calculated based on total area hauled by the plankton net and volume of water filtered was measured by the following equations: Figure 1. Map of the study area showing sampling location (Stations 1 to 5) in Batang Lupar and Batang Sadong estuaries, Sarawak, Malaysia
  • 3. BIODIVERSITAS 21 (9): 4022-4033, September 2020 4024 The volume of water filtered through the zooplankton net was calculated by the equation of, The volume of filtered water (m3 ) Where, r: radius of the mouth of the plankton net (m), and pie: 3.142, d: Length of the water column traversed by the net. Total hauling area (d): 1 meter *flow meter reading (5 rotor count is equal to 1 m)/flow meter standard. Then the abundance of zooplankton was calculated by the following equation: The abundance of zooplankton (individual/m³) = Collection of ecological samples and analysis of ecological parameters In-situ parameters of surface water were measured in all stations, including temperature, salinity, pH, dissolved oxygen, conductivity, and turbidity by using multi- parameter (Model Hydro-lab, WQC-24). Water samples were collected randomly from the water surface of river estuary from three sampling areas (replications) of a station by following Environmental Protection Agency guidelines, EPA (2008). In the laboratory, water nutrients including total suspended solids (TSS), chlorophyll a, ammonia (NH3), nitrate (NO3), phosphate (PO4) and Silica (SiO2) analyzed. Water nutrients were analyzed by APHA standard methods (2005) in the laboratory. The data of zooplankton diversity and other ecological factors were transformed and performed the normality test. normality Then a two-way ANOVA was performed on various abiotic factors and zooplankton groups to find out the variations in physicochemical parameters, population density, species diversity, and diversity index. The Shannon-Wiener index (H´) was used to summarize the information on the relative abundance of zooplankton found within the study area. The relationship between physicochemical parameters and population abundance of zooplankton was analyzed using the Canonical Correspondence Analysis (CCA). Zooplankton abundance according to stations were classified using cluster analysis, and similarity (ANOSIM) by using MVPS 3.1 and PAST (3.0) version software. RESULTS AND DISCUSSION Zooplankton diversity A total of 29 zooplankton species was recorded in the present study which belongs to 14 major groups of zooplankton (Table 1) represented by Copepoda, Crustacean nauplii, Fish larvae, Mollusca, Luciferidae, Cnidaria, Ostracoda, Cirripedia, Polychaete larvae, Chaetognatha, Appendicularia, Amphipoda, Echinodermata larvae and Cladocera. Table 1. Major groups of zooplankton at toli shad breeding ground area, in Sarawak, Malaysia Phylum Class Order Family Genus Arthropoda Hexanauplia Calanoida Paracalanidae Acrocalanus spp. Paracalanus spp. Bestiolina spp. Centropagidae Centropages spp. Acartiidae Acartia spp. Pontellidae Labidocera spp. Calanidae Canthocalanus spp. Cosmocalanus spp. Cyclopoida Oithonidae Oithona spp. Corycaeidae Corycaeus spp. Harpacticoida Tachidiidae Euterpina spp. Cirripedia larvae Malacostraca Amphipoda Gammaridea Amphipod spp. Decapoda Sergestidae Acetes spp. Isopoda Isopod Crustacea Shrimp larvae. Zoea Nauplii Ostracoda Ostracod Branchiopoda Cladocera Mollusca Bivalvia Bivalve larvae Gastropoda Gastropod larvae Chordata Actinopterygii Stomiiformes Stomiidae Lucifer Appendicularia Copelata Oikopleuridae Oikopleura Fish larvae and Fish egg Chaetognatha Sagittoidea Aphragmophora Sagittidae Sagitta spp. Annelida Polychaeta Polychaete larvae Cnidaria Cnidaria larvae Echinodermata Ophiuroidea Echinoderm larvae Nematoda Nematodes
  • 4. AIMAN et al. – Zooplankton community structure of a tropical estuary 4025 Percentage of zooplankton group from Tenualosa toli breeding area The present study reported that copepods were the major group (88.38%) of species during the whole study period, and non-copepods comprised 11.62% in the total species counted. Non-copepod comprised with Crustaceans larvae (5.88%), Chaetognatha (2.32%), Mollusca (1.95%), Polychaeta (0.88%), Cnidaria (0.19%), Fish larvae (0.13%) and others (0.27%) groups from this Batang Lupar river estuary (Figure 2). Zooplankton abundance The total population densities of zooplankton ranged from 447.5 to 27812.9 ind/m³ representing from five stations (Figure 3), and the dominant group, copepod contributed about 477.37-25921.89 ind/m3 . Zooplankton abundance in station 1 was higher (8460.72 ind/m³) followed by station 2 (5479.80 ind/m³), station 3 (4571.95 ind/m³), station 4 (4394.2 ind/m³) and station 5 (4156.73 ind/m³) (Figure 4). The highest total means zooplankton abundance (10070.39 ind/m³) was recorded in December 2016 while the lowest abundance (1461.47 ind/m³) was observed in July 2016 (Table 2). The abundance and distribution of zooplankton at all stations showed that copepod was the dominant group in terms of composition (Figure 5). Copepod showed 86.05%, 90.57%, 82.40%, 90.82% and 94.41% in total zooplankton population in stations 1, 2, 3, 4 and 5, respectively. Second important group was Crustacean nauplii (2.45% to 9.38%) followed by Chaetognatha (0.30% to 6.64%) and Mollusca (0.12% to 3.87%). Ecological parameter Water salinity and conductivity were significantly different (p<0.05) in all stations; while, these values were found higher at stations 1, 2, and 3 but lower at stations 4 and 5 (Table 3). Salinity (16.48 to 46.97 PSU) and conductivity (24.66 to 57.52 S/m) were the higher at stations 1, 2, and 3 in July, August, September, April, May, and June. Turbidity and total suspended solids showed almost similar trends but, not significantly (p≥0.05) different. The surface water temperature at all stations was at the range of 26.0ºC to 26.48ºC (north-west monsoon) from January to April, while in July to December recorded in higher trend from 28ᵒC to 31.39ᵒC (Figure 6). The temperature was not significantly different p≥0.05 among the station studied (Table 3). The highest water temperature was recorded (31.39ºC) in August at station 3 and the lowest (21.95ºC) in June at station 5. Figure 2. Percentage of zooplankton group from toli shad (Tenualosa toli) breeding ground area during the study period in Sarawak, Malaysia Table 2. Summary result of two-way ANOVA and Tukey HSD tests on various zooplankton groups (mean (ind/m³)±SE) Zooplankton Station 1 Station 2 Station 3 Station 4 Station 5 Copepoda 7301.84±2075.13a 4277.8±1265.4a 3854.4±605.9a 3955.6±908.6a 4197.8±1152.7a ns Crustacean nauplii 618.15±228.22a 230.93±81.2a 438.95±185.7a 171.83±107.4a 108.95±41.5a ns Fish larvae 6.47±2.92a 13.53±5.27a 3.85±1.25a 6.32±2.08a 4.59±2.36a ns Mollusca 328.89±259.83a 33.76±11.23a 5.43±2.19a 41.26±15.07a 111.13±83.2a ns Luciferidea 1.00±0.66a 1.60±1.25a 2.31±1.79a 0.00a 0.00a ns Cnidaria 8.36±8.05a 25.65±18.31a 2.67±1.55a 12.34±6.75a 1.18±0.69a ns Ostracoda 11.12±10.89a 2.32±1.57a 2.80±2.58a 1.60±1.6a 0.00 a ns Cirripedea 10.59±9.13a 0.18±0.18a 0.46±0.46a 1.57±1.34a 2.14±1.21a ns Polychaeta 79.66±69.64a 47.90±43.94a 53.62±50.58a 46.82±33.14a 5.80±3.81a ns Chaetognatha 101.31±35.61ab 81.32±34.91ab 310.51±102.3a 113.60±71.46ab 13.28±5.66b ** Appendicularidae 16.98±10.95a 5.66±2.57a 2.53±0.98a 2.04±1.64a 0.19±0.19a ns Amphipoda 1.35±0.63a 1.10±1.1a 0.16±0.16a 2.57±2.41a 1.23±0.66a ns Echinodermata 0.40±0.0 0a 1.28±1.28a 0.00a 0.00a 0.00 a ns Cladocerans 0.00a 0.12±0.12a 0.00a 0.00a 0.00 a ns Note: *Correlation is significant at 0.05 level (2-tailed). **Correlation is significant at 0.01 level (2-tailed)
  • 5. BIODIVERSITAS 21 (9): 4022-4033, September 2020 4026 Water pH was significantly different p<0.01 in all stations. Riverine and estuarine water were alkaline (7.0 to 8.25) at all stations in July, August and September, while from October to June it was slightly acidic (stations 1 to 3) to alkaline (stations 4 and 5), and ranged from 6.75 to 7.5. Dissolved oxygen (DO) was significantly different (p<0.05), and found higher in May and June at stations 1 to 3 (5.27 to 10.6 mg/l) and lower in other months in other stations with the range of 3.0 to 6.25 mg/l. The maximum mean value of total suspended solids was found at station 1 in July (0.83 mg/l), while the lowest value at station 2 in November (0.06 mg/l), but not significantly different at all stations. Chlorophyll a ranged from 0.001 to 0.07 mg/l) during the study period. Water nutrients (ammonium, nitrate, phosphate), total suspended solids, chlorophyll a, and silica showed a non-significant trend (p≥0.05) (Table 3) in all stations (Figure 7). Ecological indices The richness index (1.07 to 1.54) was higher at station 2 where 13 zooplankton groups and lowers at station 5 which comprised nine zooplankton groups. Both the Shannon and evenness indices were the highest at station 3 and the lowest at station 5 which Shannon indices were within the range of 0.28 to 0.64 and evenness indices were within 0.12 to 0.26 (Figure 8). ANOSIM analysis of zooplankton population abundance The similarity of zooplankton abundance among all stations based on the number of zooplankton found per m3 data (permutation: 9999) revealed that there were no significant differences (p< 0.30) among stations. The study also revealed that some stations that were located in a similar habitat shared high similarity in abundance among the stations. The study revealed, station 1 was very similar with station 2 (similarity index: 0.18), and very dissimilar with station 3 (similarity index: 0.32); station 2 was very similar with station 3 (similarity index: 0.11), and very dissimilar with station 4 (similarity index: 0.43); station 3 was very similar with station 2 (similarity index: 0.11), and very dissimilar with station 5 (similarity index: 0.61); station 4 was very similar with station 1 (similarity index: 0.25), and very dissimilar with station 3 (similarity index: 0.62); station 5 was very similar with station 2 (similarity index: 0.29), and very dissimilar with station 3 (similarity index: 0.67) (Table 4). Table 3. Summary results of two-way ANOVA and Tukey HSD tests on various abiotic factors (mean±SE) Parameter Station p Station 1 Station 2 Station 3 Station 4 Station 5 Salinity (psu) 22.265±2.24ᵃᵇ 26.85±2.56ᵃ 16.58±1.28ᵇ 8.77±1.21ᶜ 5.66±0.95ᶜ * Conductivity (S/m) 34.993±3.22ab 41.94±3.39a 27.01±1.88b 15.01±2.03c 9.89±1.55c * Temperature (⁰C) 27.65±0.71a 27.61±0.73a 28.61±0.74a 28.36±0.82a 27.812±0.8a ns pH 7.363±0.13ᵃᵇ 7.63±0.12a 7.36±0.13ab 6.996±0.17b 7.02±0.16b ** Turbidity (NTU) 181.75±38.60a 186.57±17.80a 135.98±14.8a 204.7±32.39a 196.27±22.0a ns DO (mg/L) 5.011±0.50ab 6.17±0.46a 4.99±0.27ab 4.21±0.21b 4.42±0.25b * TSS (mg/L) 0.728±0.18a 1.14±0.52a 0.58±0.15a 0.42±0.15a 0.699±0.2a ns Chlorophyll a (mg/L) 0.016±0.01a 0.01±0.003a 0.009±0.003a 0.01±0.003a 0.006±0.002a ns NH3 (mg/L) 0.0675±0.01a 0.062±0.008a 0.057±0.006a 0.061±0.007a 0.053±0.006a ns NO₃-N(mg/L) 0.018±0.002a 0.013±0.002a 0.012±0.002a 0.014±0.002a 0.012±0.002a ns PO4-P(mg/L) 0.023±0.008a 0.025±0.007a 0.025±0.006a 0.021±0.005a 0.023±0.005a ns SiO (mg/L) 10.78±0.81a 11.132±0.47a 10.968±0.36a 10.65±0.90a 10.397±0.76a ns Note: *Correlation is significant at 0.05 level (2-tailed). **Correlation is significant at 0.01 level (2-tailed). Figure 3. The monthly zooplankton abundance (ind/m³) at Batang Lupar and Batang Sadong (Sarawak, Malaysia) estuarine complex during the study period
  • 6. AIMAN et al. – Zooplankton community structure of a tropical estuary 4027 Figure 4. The monthly average abundance of total zooplankton from Batang Lupar and Batang Sadong estuaries, Sarawak, Malaysia during the study period Figure 5. Percentage of the zooplankton group from July 2016 until June 2017 in the study areas (ST1-ST5)
  • 7. BIODIVERSITAS 21 (9): 4022-4033, September 2020 4028 Figure 6. The monthly water quality parameter (in-situ ecological parameter) in Batang Lupar and Batang Sadong estuaries, Sarawak, Malaysia during the study period Inter-station cluster analysis Cluster analysis of zooplankton abundance in all 5 stations revealed a clear inter-stational grouping. The dendrogram presented the zooplankton density in total number of stations (5) were generally classified into 2 groups at the similarity level of 0.90 based on the difference of stations (Figure 9). Station 1 was clearly separated from another cluster comprised of Stations 2-5. Canonical correspondence analysis (CCA) The first canonical axis accounted for 44.65% and the second axis accounted for 25.17% of the variance in the zooplankton abundance. Thus the first two axes cumulatively explain 69.82% of the variance. The third canonical axis accounted for 21.42% and altogether the value represents 91.24%. CCA model confirmed that key abiotic factors notably Turbidity and nitrate (NO3-N) were highly correlated with individual groups of zooplankton abundance. Here, ecological parameters such as Turbidity (eigenvalue: 0.044) and nitrate (eigenvalue: 0.025) were highly correlated among all other parameters (Figure 10). Zooplankton groups Cirripedia larvae, mollusks, amphipods, were found to be closely associated with turbidity content of water (Figure 10).
  • 8. AIMAN et al. – Zooplankton community structure of a tropical estuary 4029 Figure 7. The monthly water quality parameters in Batang Lupar and Batang Sadong estuaries, Sarawak, Malaysia during the study period Figure 8. Diversity, evenness and richness index of zooplankton at Batang Lupar and Batang Sadong estuaries, Sarawak, Malaysia
  • 9. BIODIVERSITAS 21 (9): 4022-4033, September 2020 4030 Table 4. The similarity of zooplankton population abundance analyzed by one-way ANOSIM (PAST-3.25) during study periods for 5 stations S1 S2 S3 S4 S5 S1 0.176 0.326 0.251 0.298 S2 0.175 0.112 0.433 0.291 S3 0.326 0.112 0.617 0.671 S4 0.251 0.431 0.617 0.575 S5 0.298 0.291 0.671 0.575 Figure 9. Dendrogram based on Bray-Curtis similarity between of zooplankton density in different stations in the study area Figure 10. Canonical correspondence analysis (CCA) ordination depicting relationships among abundances of zooplankton and environmental variables
  • 10. AIMAN et al. – Zooplankton community structure of a tropical estuary 4031 Table 5. Comparison of zooplankton abundance with other studies in Malaysia Habitat Zooplankton Mesh size Reference Marudu Bay estuaries 1243 to 1553 ind/m3 20 μm Tan and Ransangan (2017) Lukut estuary, Negeri Sembilan 104300 ind/m3 150 μm Musa and Singh (2015) Merbok estuary Kedah 361×103 ind/m3 150 μm Fatema and Omar (2016) Seagrass meadow Johor, Malaysia 17.0 x104 ind/m3 100 μm Matias-Peralta and Yusoff (2015) Seagrass bed, Merambong shoal 3030.16 to 4006.5 ind/m³ 140 μm Azmi et al. (2016) Mangrove estuary, Malaysia 12330 - 20311 ind/m3 180 μm Chew and Chong (2011) Coast of Klang Strait, Malaysia 30951-55756 ind/m3 180-363 μm Chew and Chong (2016) Borneo coastal waters 232 to 251 ind/m3 0.03 mm Jivaluk (1999) Seagrass bed, Pulau Tinggi, Johor 1245 ind/m3 100 μm Shuaib et al. (2019) Straits of Malacca 9202 ind/m3 140 μm Rezai et al. (2011) Batang Lupar and Batang Sadong estuary, Sarawak 447.5 to 27812.9 ind/m³ 150 μm Present study Discussion The research focused on the studies of zooplankton recently due to its functions in the aquatic ecosystems as live food and a contributor to the secondary consumers of the riverine ecosystem. Zooplankton also plays a key environmental indicator in any aquatic ecosystem as well as works an important role in the aquatic food chain. A total of 29 spp. with 14 major groups of zooplankton was recorded in the present study, which is a moderate number of species compared to other studies; that is lower than the value recorded (91 spp.) by Chew et al. (2015) in coastal estuaries, Abu Hena et al. (2016) in mangrove estuary (33 sp.) and Tinggi and Sibu Islands (129 sp.) Malaysia (Metillo et al. 2018), and higher than the value of Straits of Johor (Kassim et al. 2015) and Sungai Lukut (Musa and Singh 2015). A comparison of the zooplankton number and abundance of the present study with other studies is presented in Table 5. The range of total abundance of zooplankton was found from 447.5 to 27812.9 ind/m³ representing from 5 stations, which is coincided with the findings from some coastal and estuarine waters (Table 5). The abundance of zooplankton recorded from these 2 estuarine habitats was higher than that of (232±125 ind/m3 ) reported by Jivaluk (1999) in Sabah, Sarawak and Brunei Darussalam waters and comparable to that of recorded in Matang mangroves, Marudu Bay estuaries and Straits of Malacca (Table 5). Generally, different estuarine and coast have a different environmental setting (Blaber 1997) due to the different tidal range, freshwater input, geomorphology, and human pressure (McLusky and Elliott 2004), which can also be driving force in a variation of the abundance of zooplankton in a different regime. Studies revealed that crustaceans, especially copepods form a major portion of the zooplankton community in most of the estuarine regime (Abu Hena et al. 2016). In the present study, copepods were found occupying 88.38% of the total zooplankton, which is lower than that of 94.7% reported by Zulikha et al. (2013) in Perak river, Malaysia. In the context of the number of species, the present finding revealed lower than that of 49 species identified from the Bintulu coast (Johan et al. 2013) and 48 species in Sangga estuary, Malaysia (Chew and Chong 2011). It is assumed that different factors such as sampling apparatus, duration, and area of coverage could attribute to the different findings regarding species composition (Johan et al. 2013). Calanoida constituted a large number of species of copepod in the present study, which coincided, with the findings of Johan et al. (2012) probably due to their continuous breeding behavior, quick larval development and the adaptation to the widely changing environment in the estuary (Perumal et al. 2009). Copepod contributes about 477.37-25921.89 ind/m3 , and 88.38% of total zooplankton followed by crustacean larvae 5.88%, Chaetognatha 2.32%, Mollusca 1.95%, Polychaeta 0.85% and others (0.59%). Zooplankton abundance was higher (8460.72 ind/m³) in station 1 followed by station 2 (5479.80 ind/m³), station 3 (4571.95 ind/m³), station 4 (4394.2 ind/m³) and station 5 (4156.73 ind/m³). It is probably due to higher nutrient input in station 1 from adjacent mangrove ecosystems as noticed by other studies elsewhere (Abu Hena et al. 2016). The highest total means zooplankton abundance (10070.39 ind/m³) was recorded in December 2016 while the lowest abundance (1461.47 ind/m³) was observed in July 2016. The higher abundance of zooplankton in December could be directed by nutrient supply due to higher precipitation in this area, which provides a favorable condition for zooplankton development (Abu Hena et al. 2016). This finding is similar to the studies of Yoshida et al. (2012); Chew et al. (2015); Kassim et al. (2015) and Tan and Ransangan (2017) in other tropical and sub-tropical coasts. Species richness index (1.07 to 1.54) was higher at station 2 (1.54) which referred to the higher number species that was found in the downstream area, and populated by a diverse salinity tolerant species found in the mouth of the estuary. In the upstream area (station 5), a lower richness index (1.07) was recorded and these areas were dominated by freshwater species. The Shannon index was higher at station 3 (0.64) and lower at station 5 (0.27) while the Evenness index was 0.25 and 0.12 respectively. These indices showed that the species homogeneity of the downstream area stations (station 3) was higher because this station represented the end-point of downstream areas and the start-point of upstream areas. Station 5 (upstream) showed lower homogeneity of species; zooplankton species assemblage of these areas was very scattered. These are similar to the findings of Abu Hena et al. (2016) and Ismail
  • 11. BIODIVERSITAS 21 (9): 4022-4033, September 2020 4032 and Zaidin (2015). The present study also revealed that the zooplankton composition was similar between some stations and these stations were considered sharing a similar habitat (Table 4). A similar observation was also found by Favier and Winkler (2014) at St Lawrence estuarine transition zone, Chen and Liu (2015) in the Yellow Sea and the East China Sea and Bhat et al. (2014) at tropical wetland India. Cluster analysis of zooplankton abundance in all five stations revealed a clear inter-stational grouping. The dendrogram presented the zooplankton abundance in the total number of stations (5) were generally classified into 2 groups at the similarity level of 0.90 based on the difference of stations. The cluster analysis of the present study was very relevant with the study of Johan et al. (2012) at Perai river estuary, Penang, Malaysia, and Razak et al. (2016) at tropical mangrove estuary in the Straits of Malacca, Malaysia. Based on CCA, there was no similarity between ecological and zooplankton abundance with the present study. However, Metillo et al. (2018) showed the same sort of CCA elsewhere. The present study found that copepod was the dominant group in the abundance and composition of zooplankton could probably due to good environment support because these species are very useful for coastal and estuarine fishery resources in this estuarine environment and associated with water turbidity and nitrate. The rivers of Sarawak harbors diverse groups of zooplankton and could have significant contributions on the breeding ground for different fish species. Different ecological parameters were influenced the zooplankton abundance, diversity, and distribution. The zooplankton population in the Tenualosa toli habitat exhibited some degree of population diversity, stable uniformity, and evenly distributed. 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