Ocean Science Journal (2024) 59:19 Online ISSN 2005-7172

https://doi.org/10.1007/s12601-024-00142-5 Print ISSN 1738-5261

ARTICLE

Dinoflagellate Cyst Assemblage, Abundance and Distribution in Three

Estuaries in Bone Bay, South Sulawesi, Indonesia
Nita Rukminasari1 · Sapto Andriyono2 · Andi Aliyah Hidayani1

Received: 3 July 2023 / Revised: 3 December 2023 / Accepted: 8 February 2024

© The Author(s), under exclusive licence to Korea Institute of Ocean Science & Technology (KIOST) and the Korean Society of Oceanography (KSO) and
Springer Nature B.V. 2024

Abstract
Dinoflagellates are the main group of primary producers in freshwater and marine ecosystems. Some of these species can
produce toxins (only 10% from the total species) and cause the occurrence of harmful-algal-blooms (HABs) worldwide.
The purpose of this study was to examine the species assemblages, distribution, diversity, species richness, and abundance
of dinoflagellate cysts in three estuaries around Bone Bay, Sulawesi, Indonesia. Thirty-six surface sediment samples were
collected from the Teko, Tangka and Panyula estuaries, and dinoflagellates cysts were counted and identified. Multivariate
analyses were conducted to examine species assemblages, diversity and richness. Eighteen dinoflagellate taxa from 11 genera
and 8 families were identified. The three most abundant dinoflagellate species were Alexandrium minutum, Pentapharsod-
inium tyrrhenicum, and Scrippsiella lachrymosa. Species assemblages varied between sampling sites, there was no shifting
from autotroph to heterotroph dinoflagellate cysts, and based on species richness and diversity, Bone Bay was categorized as
oligotrophic. These findings indicate that cyst species could be good indicators for eutrophication and industrial pollution,
even though eutrophication was not detected at the sites in Bone Bay during the research period.

Keywords Dinoflagellate cyst · Distribution and assemblages · Bone Bay · Indonesia

1 Introduction Dinoflagellates are highly diverse, comprising both pho-

Dinoflagellates are a group of protists that are bi-flagellated
and unicellular (Baxter et al. 2008). Red tides are a phe-
nomenon caused by the blooming of dinoflagellates, some
of which produce toxins (Shen et al. 2010). During their life
cycle, dinoflagellates can form cysts to survive in unfavora-
ble environmental conditions. The cysts, also called dino-
cysts, are protected by a membrane of highly resistant poly-
mers called dinosporin, enabling the cysts to be preserved in
sediment layers (Ribeiro and Amorim 2008). Dinoflagellate
cysts in both past and modern assemblages have been used
as bioindicators for changes in several environmental param-
eters such as sea-surface temperature, salinity, sea-ice cover
duration, and productivity (Richerol et al. 2012).
* Nita Rukminasari
nita.r@unhas.ac.id
1
Faculty of Marine Science and Fisheries, Hasanuddin
University, Sulawesi Selatan 90245, Indonesia
2
Faculty of Fisheries and Marine, Airlangga University,
Jawa Timur 60115, Indonesia
totropic autotrophs and heterotrophs, and this phytoplank-
ton group plays an important role in marine and freshwater
ecosystem productivity (Schenepf and Elbrachter 1992).
Furthermore, dinoflagellates have developed complex nutri-
tional strategies (Stoecker 1999). Many dinoflagellates are
meroplanktonic, and also develop a resting stage or cyst
(dinocyst) as part of their life cycle (Dale et al. 2002).
The analysis of surface sediment samples to examine the
changes in dinocyst assemblages by Harland et al. (2004b)
and Wang et al. (2004) found that complex interactions with
environmental conditions could influence temporal varia-
tions in the composition of dinocyst assemblages. Harland
et al. (2004a, b) found that seasonal cyst abundance patterns
could be determined by water stability and nutrient availabil-
ity. These studies indicate that cyst production patterns are
complex and unpredictable ecological processes require that
long-term surveys are carried out to collect representative
data to detect temporal scales of variation at several levels,
e.g. individual, population and community levels.
In general, dinoflagellate cyst morphology is species-
specific and dinocysts can be identified based on several

Vol.:(0123456789)
 19 Page 2 of 13
characteristic traits such as their shape and size, ornamenta-
tion of or processes arising from the cyst surface, wall struc-
ture and color, and archeopyle type (Matsuoka and Fukuyo
2000; Zonneveld and Pospelova 2015). These characteris-
tics of cyst morphology and structure are widely considered
essential features for cyst identification, although diversity in
such morphological characteristics is observed more often
in organic-walled cyst morphotypes than in calcareous cysts
(Narale 2016). Notably, there can be considerable variation
in cyst morphological characteristics within a single species.
The most distinctive traits of dinoflagellate cysts are those
related to the structure and composition of the cyst wall. The
temporary or pellicle cysts can be distinguished from resting
cysts by the absence or presence of a thick wall. The outer
layer of a pellicle cyst is usually thin, while in resting cysts
there are one, two or three moderately thick to very thick cell
wall layers (Kremp 2013).
Factors that can influence cyst formation such as seawater
temperature, salinity, density and nutrient concentrations,
can also affect the morphology of resting cysts (Mertens
et al. 2011, 2012). In addition, eutrophication, sea-surface
temperature, salinity, and coastal upwelling events are all
factors that can affect dinoflagellate species composition and
distribution (Dale et al. 1999; Pospelova et al. 2002).
Heterotrophic dinoflagellates have varied feeding strate-
gies and prey preferences (Hansen 1991; Hansen and Calado
1999; Jacobson and Anderson 1986), thus the abundance
and species composition of heterotrophic dinoflagellates
could be influenced by nutrient concentrations, and therefore
by eutrophication. In addition, the response of dinoflagellate
cysts to eutrophication in coastal waters is also influenced by
the physical and environmental characteristics of estuaries
(Pospelova et al. 2002). Dinoflagellate cyst assemblages in
estuaries vary by biogeographic province; however, within
each biogeographic province the estuary type will influence
dinoflagellate cyst assemblages (Price et al. 2016).
This study was motivated by the lack of studies on the
characteristics of dinoflagellate cyst assemblages in Bone
Bay, South Sulawesi, Indonesia. We studied the diversity,
overall and relative abundance, and dinoflagellate cysts col-
lected from recently deposited surface sediments in the estu-
aries of three rivers flowing into Bone Bay (Teko, Tangka
and Panyula river estuaries). The main purpose of the study
was to examine the differences in dinoflagellate assemblages
across these three estuaries in Bone Bay.
2 Material and Methods
2.1 Study Site
The Gulf of Bone, also known as Bone Bay, is the seaway
enclosed between the south and southeast peninsulas of the
Ocean Science Journal (2024) 59:19
island of Sulawesi in Indonesia and opens to the south into
the Flores Sea (Ambo-Rappe and Moore 2019). The study
sites were three estuaries at Bone Bay, namely Teko Estuary
(Bulukumba Regency), Tangka Estuary (Sinjai Regency),
and Panyula Estuary (Bone Regency) (Fig. 1). Sediment
samples were collected from four stations within each estu-
ary, with three replicates per station.
2.2 Sediment Sample Collection and Preparation
Surface sediments were collected using a Wilder Hand Corer
from the four sampling stations in each of the three estuaries
in Bone Bay (Fig. 1) during July 2022. At each station, three
replicate surface sediment samples were collected from the
top 2 cm of the sediment layer. The samples were stored at
4 °C in dark conditions to ensure that cyst germination did
not occur before the samples were processed. To obtain the
whole cyst assemblage, chemical substances were not used
on the sediment samples. A 4–5 g sediment was put into
a small Baker glass and then 50 ml filtered seawater was
added. The sediment samples were then sonicated for 5 min
in an ultra-sonic bath and then wet-sieved through 250 µm,
100 µm and 20 µm-mesh sieves using filtered seawater. The
last remaining fraction left on the 20 μm sieve was washed
off the sieve using filtered seawater. The 20 µm fraction was
used for further analysis.
2.3 Assemblage Composition
To identify the dinoflagellate cysts present, 1 ml of each
sample was dropped onto a hemocytometer, and then
observed with a light Microscope (Binocular Olympus
CX23 LED) with a magnification of × 40 to × 100. Photo-
graphs were taken using a Canon EOS M10 camera. Empty
cysts and cysts with cell contents were both counted and
recorded by species. Dinoflagellate cyst identification fol-
lowed references (Alkawri 2016; Aydin et al. 2011; Bravo
et al. 2006; Godhe et al. 2000; Joyce et al. 2005; Mohamed
and Al-Shehri 2011; Narale and Anil 2017; Nehring 1997;
Pospelova et al. 2004; Shin et al. 2011; Uddandam et al.
2017). The parameters derived from the data were the cyst
morphotype composition, species diversity (Shannon–Wie-
ner’s Diversity index (H’) and evenness (Shannon and
Weaver 1949).
2.4 Creating a Dinoflagellate Cyst Distribution Map
To create a dinoflagellate cyst distribution map, each sam-
pling point is taken by taking the coordinates using GPS.
Each coordinate point that already has a cyst value is then
analyzed spatially to get the cyst distribution value in the
waters. Analysis of data on the distribution of cysts in the
waters was conducted using interpolation techniques with
Ocean Science Journal (2024) 59:19
Fig. 1  Geographical location
of the sampling stations within
Bone Bay. Yellow dots indicate
the sampling stations
the Inverse Distance Weighting (IDW) method. The IDW
method directly adopts the assumption that things that are
close to each other are more similar than things that are
far apart. To estimate a value at each unmeasured location,
IDW will use the measurement values that surround the
location to be estimated. In the IDW method, it is assumed
that the degree of correlation and similarity between the
estimated points and the estimator’s data is proportional to
the distance. The weight will change linearly, as a function
of distance, according to the distance to the estimator data
(Almasi et al. 2014). This weight is not affected by the posi-
tion or location of the estimating data with other estimating
data.
2.5 Data Analysis
Diversity analyses followed Rukminasari and Tahir (2021).
Two-way analysis of variance (ANOVA) was implemented
in GraphPad Prism 7 to evaluate the significance of differ-
ences in dinoflagellate cyst abundance and diversity indices
at the 95% confidence level (α = 0.05). Non Metric Mul-
tidimensional Scaling (nMDS) analysis was conducted
in PRIMER Ver. 5 (PRIMER–E Ltd. Plymouth, UK) to
evaluate the differences in dinoflagellate cyst assemblages
between the three sites. To analyze the relationships between
Page 3 of 13 19
sets of categorical variables (family of dinoflagellate cyst
abundance) and environmental variables (salinity, tem-
perature, DO, TDS, C Organic, C Inorganic and N-total),
Canonical Correspondence Analysis (CCA) was performed
using XLSTAT 2019 version.
3 Results
3.1 Abundance, Species Richness and Diversity
Index of Dinoflagellate Cysts
Dinoflagellate cyst abundance differed between and within
the three sampling sites (Teko, Tangka and Panyula estuar-
ies) (Fig. 2). The sites with the highest (289 cysts/g) and
the lowest (162 cysts/g) mean dinoflagellate cyst abun-
dance values were in Tangka Estuary (Sinjai Regency) and
Teko Estuary (Bulukumba Regency), respectively (Fig. 2).
The dinoflagellate cyst abundance also varied significantly
(P < 0.05) between stations at two sites. Station II differed
significantly from stations I, III and IV in the Teko Estuary,
while station IV differed significantly from stations I, II and
III in the Panyula estuary (Fig. 2).
Based on dinoflagellate cyst morphology, we identified
18 dinoflagellate cyst species (Table 1, references used in
 19 Page 4 of 13
Fig. 2  Dinoflagellate cyst abun-
dance at 12 sampling stations in
three Bone Bay estuaries. small
case superscript letters represent
significantly different values
(P < 0.05)
Table 1: Barokah et al. 2017; Furuya et al. 2010; Gurning
et al. 2020; Smayda and Reynolds 2001). These species
belonged to seven families (Gonyaulacaceae, Gymnod-
iniaceae, Osteropsidaceae, Peridiniaceae, Polykrikaceae,
Protoperidiniaceae, and Pyrophacaceae) and a group of
uncertain taxonomic lineage labelled as incertae sedis. The
number of species present varied between families and
between sampling sites (Fig. 3). Most of the dinoflagel-
late species found at all sampling sites belonged to the
Peridiniaceae family. The three most abundant dinoflagel-
late cyst species from all sampling stations combined were
Alexandrium minutum, Pentapharsodinium tyrrhenicum/
Ensiculifera tyrrhenica and Scrippsiella lachrymose, with
mean abundance values of 1321 cysts/g, 1316 cysts/g, and
1267 cysts/g, respectively (Fig. 4).
Overall, the majority (66%) of the dinoflagellate cyst
species identified were classified as autotrophic species
and 34% as heterotrophic species. Station II in the Pany-
ula Estuary had the highest percentage of autotrophic spe-
cies, while the lowest percentage was at station IV in the
Tangka Estuary (Fig. 5). Furthermore, the highest and the
lowest percentage of heterotrophic species were found at
Tangka Estuary station IV (60%) and Panyula Estuary sta-
tion III (17%), respectively (Fig. 5).
The ecological indices also varied between and within
sites. The number of dinoflagellate cyst species per station
ranged from 2 to 6. Species richness by station ranged
from 0.4147 (Tangka estuary, station II) to 0.8492 (Pany-
ula estuary, station IV) (Fig. 6a). Species richness was
highest at station I in the Tangka Estuary, and lowest at
station II in the Teko Estuary. Pileou’s evenness index (J’)
was highest at station I in the Tangka Estuary (0.99964)
and lowest at station II in the Teko estuary (0.9461)
(Fig. 6b). However, Pileou’s evenness index was generally
high and the between-site differences were not significant
Ocean Science Journal (2024) 59:19
(P > 0.5). Shannon diversity (H’) ranged from 0.5995 to
0.9964 (Fig. 6c).
3.2 Spatial Distribution of Dinoflagellate Cyst
Abundance
The spatial distribution of dinoflagellate cyst abundance var-
ied between the three sampling sites (Fig. 7). Dinoflagellate
cysts were most abundant in the river and at the river mouth
in the Tangka Estuary, while in the Teko Estuary, dinoflagel-
late cyst abundance was highest in waters further offshore.
In the Panyula Estuary, dinoflagellate cyst abundance was
distributed fairly evenly across the site, including the river,
river mouth and offshore areas.
3.3 Dinoflagellate Cyst Species Assemblages
nMDS performed with ordination using the log of dino-
flagellate cyst mean abundance for each site. The nMDS
plot (Fig. 8) shows that dinoflagellate cyst assemblages
at each site are quite spread out. The Teko and Tangka
estuaries each lie within an approximately oval shape
with no overlap. However, the Panyula Estuary sample
distribution is scattered more widely, overlapping both
the other sites, especially the Teko Estuary, and several
outliers (Fig. 8). The relatively low stress value of 0.19
indicates that the ordination gives a fairly good repre-
sentation of the distances between the assemblages. The
assemblages in Group I are mostly from the Teko Estuary
(represented by green triangles in Fig. 8) and were mainly
dominated by Alexandrium minutum, Pentapharsodinium
tyrrhenicum/Ensiculifera tyrrhenica, Cochlodinium sp.,
and Scrippsiella lachrymosa. Assemblages in Group II,
mostly from the Tangka Estuary (represented by round
symbols in Fig. 8) were dominated by Polykrikos kofoidii,
Ocean Science Journal (2024) 59:19 Page 5 of 13 19

Table 1  List of dinoflagellate cyst genera and species found at the study sites
Biological name Dinoflagellate cyct (Pal- Estuary HABs Species References
aentological name)
Teko Tangka Panyula

Dubridinium Dubridinium spp. Dubridinium spp. √

Gonyaulax Gonyaulax sp. Cyst of Gonyaulax sp. √ Smayda & Reynolds,
(2001)
Cochlodinium Cochlodinium spp. Cyst of Cochlodinium √ √ √ √ Barokah et al. (2017);
spp. Furuya et al. (2010)
Gymnodinium Levanderina fissa Cyst of Levanderina fissa √ √ Barokah et al. (2017);
Furuya et al. (2010)
Alexandrium Alexandrium tamarense Cyst of Alexandrium √ √ √ √ Barokah et al. (2017);
tamarense Furuya et al. (2010)
Alexandrium catenella Cyst of Alexandrium √ √ √ √ Barokah et al. (2017);
catenella Furuya et al. (2010)
Alexandrium minutum Cyst of Alexandrium √ √ √ √ Barokah et al. (2017);
minutum Furuya et al. (2010)
Pentapharsodinium Pentapharsodinium tyr- Unknown √ √ √ Barokah et al. (2017);
rhenicum/Ensiculifera Furuya et al. (2010)
tyrrhenica
Scrippsiella Scrippsiella crystallina Cyst of Scrippsiella √ √ √ √ Barokah et al. (2017);
crystallina Furuya et al. (2010)
Scrippsiella lachrymosa Cyst of Scrippsiella lach- √ √ √ √ Barokah et al. (2017);
rymosa Furuya et al. (2010)
Scrippsiella rotunda Cyst of Scrippsiella √ √ Barokah et al. (2017);
rotunda Furuya et al. (2010)
Votadinium Votadinium calvum Cyst of Votadinium √ Barokah et al. (2017);
calvum Furuya et al. (2010)
Polykrikos Polykrikos kofoidii Cyst of Polykrikos √ √ Furuya et al. (2010;
kofoidii Gurning et al. (2020)
Polykrikos schwartzii Cyst of Polykrikos √ √ Furuya et al. (2010;
schwartzii Gurning et al. (2020)
Preperidinium Protoperidinium leonis Cyst of Protoperidinium √ Furuya et al. (2010;
leonis Gurning et al. (2020)
Trinovantedinium appla- Cyst of Trinovantedinium √ √ Furuya et al. (2010;
natum applanatum Gurning et al. (2020)
Protoperidinium subin- Cyst of Protoperidinium √ √ Furuya et al. (2010;
erme subinerme Gurning et al. (2020)
Tuberculodinium Tuberculodinium van- Cyst of Tuberculodinium √ Furuya et al. (2010;
campoae vancampoae Gurning et al. (2020)
Total 8 10 14 14

HABs Harmful Algal Blooms

Pentapharsodinium tyrrhenicum/Ensiculifera tyrrhenica, Interestingly, the species Pentapharsodinium tyrrhenicum/

Scrippsiella lachrymosa, and Scrippsiella crystallina.
Group III from the Panyula Estuary (represented by square
symbols in Fig. 8.) was most strongly dominated by Pol-
ykrikos kofoidii, Alexandrium minutum, and Scrippsiella
lachrymose.
The nMDS, ANOSIM and SIMPER results show signifi-
cant differences in dinoflagellate cyst assemblages between
stations at each site (Table 2). SIMPER results showed that
each site was dominated by one or several species from a
particular family. Overall, the Peridiniaceae and Osterop-
sidaceae were the dominant families at all sites (Table 2).
Ensiculifera tyrrhenica was the dominant dinoflagellate cyst
at all three sites.
The pairwise between-site dissimilarity percentage ranged
from 54.90 to 65.81%. The highest dissimilarity was between
the Panyula and Tangka estuaries, with Polykrikos kofoidii as
the taxa contributing the most to the dissimilarity. Dissimilar-
ity was lowest between the Teko and Panyula estuaries, with
Scrippsiella crystallina making the largest contribution to the
dissimilarity.
 19 Page 6 of 13 Ocean Science Journal (2024) 59:19

Fig. 3  Dinoflagellate cyst com-

position by family in three Bone
Bay estuaries: a Teko Estuary; b
Tangka Estuary; and c Panyula
Estuary

Fig. 4  Abundance of dinoflagel-

late cyst species identified from
three estuaries in Bone Bay
Ocean Science Journal (2024) 59:19
Fig. 5  Proportion of heterotroph
and autotroph species at 12
sampling stations in three Bone
Bay estuaries
3.4 The Relationship Between Dinoflagellate Cyst
Family and Environmental Parameters
CCA provides insights into the complex relationships
between species distribution and environmental variables.
The CCA results are shown in Fig. 9. The abundance of the
Dinoflagellate cyst family Gonyaulacaceae at the Teko Estu-
ary (Bulukumba Regency) has a strong relation with tem-
perature, while the abundance of the Osteropsidaceae family
shows a strong relation with the concentration of dissolved
oxygen. Furthermore, the abundance of the Gymnodiniaceae
family at the Tangka Estuary (Sinjai Regency) is strongly
related to the concentration of C-organic. For the families of
Polykrikaceae and Peridiniaceae, their abundances show a
strong relationship with N-total and C-organic. Similarly, the
abundance of the Pyrophacaeae and incertae sedis families
at the Panyula Estuary (Bone Regency) strongly relates to
salinity. TDS exhibits a strong relationship with the abun-
dance of the Protoperidiniaceae family.
4 Discussion
It is well known that temperature, salinity and nutrient
availability control the distribution, abundance and species
dominance of dinoflagellate cysts (Devillers and De Vernal
2000; Vernal et al. 2001). Our study found that dinoflagel-
late cyst abundance, taxonomic composition and distribution
patterns varied between sampling sites. In general, dinoflag-
ellate cyst abundance was lower at stations in the river than
Page 7 of 13 19
at those situated at the river mouth or further offshore. At
these riverine sites, the salinity was low, in the range of 1–4
parts per thousand (data not shown). This finding indicates
that salinity may play an important role in dinoflagellate
cyst abundance and distribution at the sampling sites. This
is in line with Sildever et al. (2015) who found that dino-
flagellate cyst abundance was generally low in areas of low
salinity in the Baltic Sea (the Northern Central basin and
the Gotland basin), and suggested that salinity determined
total dinocyst abundances. We found relatively low-aver-
age dinoflagellate cyst abundance at all sampling locations
(162–289 cysts/g) compared to a similar study by Rukmi-
nasari and Tahir (2021) at three estuaries in the Makassar
Strait, where dinoflagellate cyst abundance ranged from 35
to 1135 cysts/g. One likely reason for the mostly lower dino-
flagellate cyst abundance at the Bone Bay sampling sites
could be the lower salinity compared to the Makassar Strait.
According to Kunarso et al. (2018), the waters of Bone Bay
are relatively fertile and tend to have comparatively low
salinity due to the large volumes of freshwater flowing into
the bay from rivers on Sulawesi Island. In addition, there
are exchanges of water masses from the Pacific Ocean to
the Indian Ocean through the Sulawesi Sea, Flores Sea and
the Java Sea that can affect salinity levels. The dinoflagellate
cyst abundance levels found in this study are also lower than
those reported from other estuaries and coastal seas, includ-
ing in Europe (Harland et al. 2004a), and North American
(Pospelova et al. 2004). Other studies have found that dino-
flagellate cysts abundance was commonly higher than 1000
cysts/g (Pospelova and Kim 2010) and even up to 1­ 04–105
 19 Page 8 of 13 Ocean Science Journal (2024) 59:19

Fig. 6  Ecological indices at

12 sampling stations in three
Bone Bay estuaries: a Species
richness index: d, b Pielou’s
evenness: J’ and c Shannon—
Wiener’s diversity index: H’
Ocean Science Journal (2024) 59:19
Fig. 7  Spatial distribution of dinoflagellate cyst abundance in three estuaries in Bone Bay. a Teko Estuary, Bulukumba District; b Tangka Estu-
ary, Sinjai District; and c Panyula Estuary, Bone District
Stress: 0,19
Teko Estuary
Tangka Estuary
Panyula Estuary
Fig. 8  nMDS ordination of Log (X + 1) transformation comparing the
dinoflagellate cyst assemblages in terms of total number of cysts/g
DW sediment for three estuaries in Bone Bay
cysts/g (Radi et al. 2007). The low abundance of dinoflag-
ellate cysts in this study could be related to the sediment
type, which was mostly coarse in the three estuarine sites
in Bone Bay. According to Dale (1983), dinoflagellate cysts
could not settle in coarse sediment, and consequently this
Page 9 of 13 19
type of sediment was not conducive to the accumulation of
dinocysts.
Dinoflagellates are found in two distinct environments:
within the water column as part of the plankton community
and at the bottom of aquatic ecosystems, where they are
considered benthic organisms (Bralewska and Witek 1995).
Furthermore, they explained that within this taxonomic
group, there is an extraordinary variety of trophic types,
ranging from entirely autotrophic species to mixotrophs and
fully heterotrophic organisms, including parasites. Each of
these categories comprises numerous individual species.
The dinoflagellate cyst species that were abundant in the
three Bone Bay estuaries were Alexandrium minutum and
Scrippsiella lachrymose that are mixotrophic species and
Pentapharsodinium tyrrhenicum/Ensiculifera tyrrhenica that
is an autotrophic species. Furthermore, 66% of dinoflagellate
cyst species were autotrophic species, consistent with the
classification of Bone Bay as a fertile water body and one
of the upwelling areas in Indonesian waters. Autotrophic
 19 Page 10 of 13 Ocean Science Journal (2024) 59:19

Table 2  Results from nMDS ANOSIM Pairwise test and SIMPER analyses comparing dinoflagellate cyst assemblages between the three study
sites: Global R, Significance level/P value, Dissimilarity (%) and the taxa most responsible for dissimilarity
Pairwise SIMPER Results
Dissimilarity (%) 3 taxa most responsible for the
difference (%)

Teko Estuary vs Tangka Estuary 62.49 Polykrikos kofoidii (19.73)

Alexandrium minutum (13,88)
Cochlodinium spp (11.10)
Teko Estuary vs Panyula Estuary 54.9 Scrippsiella crystallina (11.57)
Cochlodinium spp (11.48)
Scrippsiella lachrymosa (11.08)
Panyula Estuary vs Tangka Estuary 65.81 Polykrikos kofoidii (19.35)
Alexandrium minutum (12.03)
Scrippsiella crystallina (11.08)
Pairwise ANOSIM Results
Global R Level of significance/P value

Teko Estuary vs Tangka Estuary 0.478 0.001

Teko Estuary vs Panyula Estuary 0.018 0.27
Panyula Estuary vs Tangka Estuary 0.339 0.001

Fig. 9  Biplot visualization of CCA Map / Symmetric

CCA to show the relationship (axes F1 and F2: 100.00 %)
between family dinoflagellate 1.2
cyst abundance (Incertae sedis, Sites
Gonyaulacaceae, Gymnodini- 1 Gonyaulacaceae Objects
aceae, Osteropsidaceae, Peri- Variables
Osteropsidaceae
diniaceae. Polykrikaceae, Proto- 0.8
peridiniaceae, Pyrophacaceae)
and environmental variables 0.6
(Temperature, Salinity, DO, Gymnodiniaceae
TDS, C_Organic, C_Inorganic, 0.4
F2 (28.94 %)

N_Total) within sites

0.2 DO
BL.I
BL.IV
BL.III
BL.II
Protoperidiniaceae Temperature
0 TDS C_Inorganic
SJ.I
SJ.II
SJ.III
Salinity BN.I
BN.III
BN.II SJ.IV
BN.IV
-0.2
N_Total
C_Organic Polykrikaceae
-0.4 Peridiniaceae

-0.6 pyrophacaceae
Incertae sedis
-0.8
-1.5 -1 -0.5 0 0.5 1 1.5
F1 (71.06 %)

dinoflagellate taxa have been utilized as indicators of long-
term variations in productivity, especially changes related to
upwelling intensity (Kim et al. 2010; Mertens et al. 2009).
The low percentage of heterotrophic dinoflagellate cysts in
this study was probably due to unfavorable nutrient condi-
tions in the water column and sediment for this dinoflagel-
late cyst group. This would be consistent with the findings
of Kim et al. (2012) that low concentrations of heterotrophic
dinoflagellate cysts in shelf sediment were due to nutrient
concentrations that were not favorable for heterotrophic
species.
Dinoflagellates cysts have been used as biological indica-
tor for both modern and past environments. Diversity indices
that have commonly been used include species assemblage
Ocean Science Journal (2024) 59:19
characteristics, diversity (Pospelova et al. 2002), and species
richness (Pospelova et al. 2002). Rodrigues et al. (2019) also
used dinoflagellate cysts to assess water quality to examine
seasonal patterns of pollution and eutrophication, using the
Shannon–Wiener diversity index as a pollution index in dia-
tom communities. Meanwhile, Pospelova et al. (2002, 2005)
used dinoflagellate cyst-based Fisher’s α and species rich-
ness as indicators of environmental conditions in estuarine
systems. In general, the less polluted the waters, the higher
the diversity index and species richness. The dinoflagellate
cyst species richness index (0.60–0.99) at the study sites
in Bone Bay can be considered relatively low compared to
studies at other sites. For example, Rukminasari and Tahir
(2021) found the species richness index at three estuaries in
the Makassar Strait ranged from 0.31–1.16. A low species
richness/diversity in this study could indicate the presence
of nutrient pollution at the sampling sites, as Pospelova et al
(2002, 2005) stated that low-dinoflagellate cyst species rich-
ness/diversity could be an indicator for nutrient pollution
and sewage outfalls. A decrease in dinoflagellate cyst species
richness can also be a signal of organic and toxic pollution
in a water body (Pospelova et al. 2005).
However, (Rodrigues et al. 2019) stated that dinoflag-
ellate abundance and diversity are mostly low in tropical
waters. Dinoflagellate diversity in this study was low (18
taxa identified from 36 samples) compared with other stud-
ies on surface sediment in coastal areas around the world
(including the Makassar Strait, South Korean coast, Izmir
Bay in the Eastern Aegean, Buzzards Bay in Massachusetts
USA, Sishili Bay in the Chinese Yellow Sea, and the south-
western Mexican coast) which mostly found more than 33
taxa (Rukminasari and Tahir 2021; Pospelova and Kim
2010; Aydin et al. 2015; Pospelova et al. 2005; Liu et al.
2012; Limoges et al. 2010). Oligohaline environments are
characterized by low cyst species diversity and abundance
(Ellegaard 2002; Mudie and Rochon 2001), while Pospelova
et al. (2004) found that dinoflagellate cyst assemblages at
low salinity stations contained less than eight taxa. There-
fore, the study results indicate that the sampling sites could
most likely be classed as oligotrophic waters.
Factors that influence dinoflagellate assemblages,
according to Rodrigues et al. (2019), include water col-
umn parameters (e.g., salinity, light, food availability) and
sediment parameters (e.g., grain size, sedimentation rates,
grazing rates, bioturbation, benthic suspension, and degra-
dation). Therefore, fluctuations in water temperature and
salinity could also cause variation in dinoflagellate cyst
assemblages. In this study, the dinoflagellate cyst assem-
blages were relatively homogenous between the stations
within each of the sampling sites (three estuaries in Bone
Bay). This may have been due to relatively small vari-
ations in environmental parameters such as temperature
and salinity between the stations. Previous studies found
Page 11 of 13 19
that when there was eutrophication from agriculture or
industrial pollution, generally accompanied by increasing
turbidity, dinoflagellate assemblage composition tended
to shift from autotrophic- dominated to heterotrophic-
dominated, as a consequence of an increasing abundance
of suitable prey (Matsuoka 1999; Pospelova et al. 2002;
Godhe and McQuoid 2003). The dominance of autotrophic
dinoflagellate cysts at all sampling stations and sites indi-
cates that there has not been a shift from autotroph to
heterotroph species in Bone Bay, and that this was likely
because environmental conditions were more favorable to
autotroph species. We argue that the results of dinoflag-
ellate cyst sampling in the three Bone Bay estuaries do
not indicate the occurrence of eutrophication or industrial
pollution, but rather most likely reflect a combination of
oligotrophic waters and coarse sediment.
5 Conclusion
This study was the first to examine the dinoflagellate
assemblages at three estuaries in Bone Bay. The study
also used dinoflagellate cysts as biological indicators of
environmental conditions in South Sulawesi coastal areas.
Our results show that dinoflagellate cyst assemblages in
Bone Bay reflect environmental differences, suggesting
that dinoflagellate cyst assemblages may be important
biotic factors in South Sulawesi coastal areas. The data
also suggested that eutrophication and industrial pollution
has not yet occurred at Bone Bay and that there had not
been a shift from autotrophic to heterotrophic dinoflagel-
late species. However, based on the species richness and
diversity, Bone Bay was categorized as an oligotrophic
water body. Salinity also appeared to be a major factor
controlling dinoflagellate cyst assemblages and their dis-
tribution at Bone Bay. Three dinoflagellate species were
present and highly abundant at all sampling sites: Alexan-
drium minutum, Pentapharsodinium tyrrhenicum/Ensicu-
lifera tyrrhenica and Scrippsiella lachrymosa.
Acknowledgements We thanks to Director of Center of Excellent and
Innovation of Seaweed Development and Utilization who has provided
us with room and facilities for analyzing our samples. Also, thanks
to Head of Bulukumba, Sinjai and Maros Regency who have given a
permission for conducting sampling in their areas. This research was
funded by Directorate Research and Community Service, Ministry of
Education and Culture, Republic of Indonesia and Universitas Hasa-
nuddin, under research scheme of Indonesian Research Collaboration
(A Scheme) with the contract number: 1377/UN4.22/PT.01.03/2022.
Author also want to thank to our students (Nur Inda Sari, Andi Widya
Anugrah, Delfira, Umi Rintin, Nurul Kiswa and Rizky Amalia Rama-
dhani) who helping us in sampling and processing our samples.
Data availability Not applicable.
 19 Page 12 of 13 Ocean Science Journal (2024) 59:19

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