Tan THetal 2016
Tan THetal 2016
Tan THetal 2016
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Abstract. A survey of marine phytoplankton in the Singapore Strait was carried out between May and June
2013, as part of an effort to determine the diversity of phytoplankton in Singapore’s coastal waters. A total of 34
microalgal samples were collected using a 20 μm-mesh plankton net and from coastal sediments. Living samples
and preserved samples in Lugol’s solution were identified to species as far as possible under the microscope. A
checklist of marine micro-phytoplankton was updated to encompass 270 taxa, including 49 new records from
Singapore waters. Some 37 species from 15 families were dinoflagellates, and 233 species from 50 families were
diatoms. Harmful microalgae, categorized as biotoxin-producers and fish killers, were also found in this survey.
These were in the genera Alexandrium, Amphidinium, Ceratium, Cochlodinium, Coolia, Dinophysis, Gambierdiscus,
Karenia, Karlodinium, Ostreopsis, Prorocentrum, Nitzschia, and Pseudo-nitzschia.
INTRODUCTION two valves. Their siliceous cell wall sets them apart
from dinoflagellates, which only have a membranous cell
Phytoplankton, or plant plankton, refers to a group of wall. Dinoflagellates possess two flagella that are used in
microscopic unicellular cells containing photosynthetic locomotion and feeding. The shapes and patterns of their
pigments that convert light energy into chemical energy thecal membranous cell walls are used in identification
for the organisms’ activity, although some species are (Steidinger & Tangen, 1997).
mixotrophic (feeding on organic or inorganic compounds
as a source of energy) or phagotrophic (feeding on other Singapore is a small country situated about 100 km north
organisms). These microscopic cells form the basis of all of the equator, with a typical equatorial climate, having
marine food webs by acting as a food source for organisms temperatures ranging from 23 to 34°C annually. Rainfall is
from higher trophic levels. They release oxygen into the water mostly uniform throughout the year and not affected by the
as a byproduct of photosynthetic activity but consume oxygen Northeast or Southwest Monsoons (National Environment
due to respiration. Micro-phytoplankton is most abundant Agency, Singapore) although some months may be drier
in coastal regions, as these organisms are dependent upon than others. As an island state located in the South China
nutrient run-off from the terrestrial environment. Diatoms Sea between the Indian Ocean and Pacific Oceans, it is
and dinoflagellates dominate the phytoplankton in the marine one of the busiest ports in the world. Despite its status as a
environment (Hasle & Syvertsen, 1997). developed country, phytoplankton diversity along the 200
km coastline of water body of this country has yet to be
The term ‘diatom’ originated from the genus name Diatoma documented. Wee (1994) compiled a marine and freshwater
De Candolle (1805). They reproduce vegetatively by phytoplankton checklist of 292 species of diatoms and two
binary fission, and most are heterovalvate, i.e., comprising species of dinoflagellates. Subsequently, Pham et al. (2011)
updated the list to 292 diatoms and 15 dinoflagellate species.
Kota Samarahan, Sarawak, Malaysia also identified and discussed in this study.
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Fig. 1. Dinoflagellates from the Singapore Strait. (A, B) Alexandrium affine (C) Gonyaulax sp. (D) Prorocentrum emarginatum (E)
Prorocentrum lima (F) Gonyaulax sp. (G) Dinophysis caudata (H) Protoperidinium pallidum (I) Prorocentrum micans (J) Ceratium furca
(K) Pyrodinium bahamense var. compressum (squashed theca plates). Scale bar = 20 µm.
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Fig. 2. Pennate diatoms from the Singapore Strait. (A) Cymbella sp. (B–E) Nitzschia sp. (F) Achnanthes sp. (G) Nitzschia sp. (H–K)
Pleurosigma sp. (L) Gyrosigma sp. (M) Rhizosolenia sp. 1. (N) Pseudo-nitzschia sp.; (O–R) Cylindrotheca sp. (S, T) Synedra sp. (U,
V) Thallasiothrix sp. (W) Bacillaria paxillifera; (X) Licmophora sp. (Y) Rhoicosphenia sp. (Z) Plagiotropis sp. (AA–AC) Nitzschia sp.
(AD, AE) Amphiprora sp 1. (AF) Achnanthes sp. (AG, AH) Navicula sp. (AI) Nitzschia sp. (AJ) Flagilariopsis sp. (AK) Nitzschia sp.
Scale bar = 20 µm.
was found in this study (Table 1). Species in the same genus reports for the first time the occurrence of C. polykrikoides
was also reported from a neighbouring country (Tan et al., in Singapore waters (Table 1).
2013b). However, no blooms or fish kill events associated
to this genus have been reported thus far. Coolia (Meunier, 1919). The five recognised species in
this genus were reported from French Polynesia, New
Ceratium (Schrank, 1793). In the dinoflagellate genus Zealand, western Mediterranean, Southwestern Indian Ocean,
Ceratium, 53 species are recognized today. Species from this Caribbean Sea, South China Sea, East China Sea, Japan
genus produce ichthyotoxins (Mijares et al., 1985) which can and Southwest Pacific Ocean (Fukuyo, 1981; Faust, 1995;
cause hypoxia and anoxia (Zingone & Enevoldsen, 2000; Rhodes & Thomas, 1997; Hage et al., 2000; Penna et al.,
GEOHAB, 2001) and are also responsible for blooms that 2005; Leaw et al., 2010). Coolia is associated with ciguatera
cause massive fish kills (Lim et al., 2012b). The occurrence fish poisoning. Its members also possess cooliatoxin that can
of this genus has been reported from China, Vietnam, and induce hypothermia by affecting sodium channel activity,
Malaysia (Gómez et al., 2010; Lim et al., 2012b; Tan et leading to respiratory failure in mice and enlargement of the
al., 2013a; Chu et al., 2014). In this study, we identified spleen (Holmes et al., 1995, Rhodes et al., 2000, Rhodes et
Ceratium furca from the Singapore Strait (Table 1; Fig. 1). al., 2014), as well as mortality in Artemia salina (Rhodes &
Thomas, 1997). Two species have previously been described
Cochlodinium (Schütt, 1896). The genus Cochlodinium and documented from Malaysia, namely Coolia tropicalis
consists of some 40 species distributed in the coastal waters and C. malayensis (Leaw et al., 2010; Mohammad-Noor et
of Southeast Asia, North America and Europe (Anton et al., 2013). However, only one species, C. malayensis, was
al., 2008, Gobler et al., 2008, Kudela & Gobler, 2012). identified in this study based on culture specimens collected
Species belonging to this genus produce ichthyotoxins as from the Singapore Strait.
well as hemolytic toxins, which can cause fish mortalities
in cage cultures (Kim et al., 1999, Gobler et al., 2008, Dinophysis (Ehrenberg, 1839). Among the 128 taxonomically
Dorantes-Aranda et al., 2009, Kudela & Gobler, 2012). The accepted species, seven species are associated with diarrhetic
same toxins also cause mortality in bivalves (Gobler et al., shellfish poisoning (DSP). Commercially important bivalves
2008), impact coral growth (Bauman et al., 2010), as well are easily exposed to and contaminated by these toxic
as affect other phytoplankton (Tang & Gobler, 2010) and species as they share similar habitats. Human consumption
zooplankton (Jiang et al., 2009; Jiang et al., 2010). Blooms of these bivalves will result in human intoxication. Patients
of Cochlodinium polykrikoides have caused sea surface intoxicated with Dinophysis toxins (DTXs) and okadaic
discoloration in Malaysia (Anton et al., 2008, Adam et acid (OA) experience gastrointestinal illness, diarrhea,
al., 2011, Lim et al., 2012b), Brunei and the Philippines nausea, vomiting, and both toxins are known to be tumor
during the Northeast monsoon (Azanza et al., 2008), with promoters (Suganuma, 1988, Vale & Sampayo, 1999, Vale
cell densities reaching up to 6 million cells L-1. This study & Sampayo, 2000). Between 1995 and 1997, six isomers of
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Tan et al.: Marine micro-phytoplankton of Singapore
Fig. 3. Centric diatoms from the Singapore Strait. (A, B) Thalassiosira sp. (C, D) Cyclotella sp. (E) Chaetoceros sp. (F–K) Coscinodiscus
sp. (L–N) Cocconeis sp. (O) Amphora sp. (P) Bacteriastrum sp. (Q) Cyclotella sp. (R) Diplomenora sp. (S) Diploneis sp. (T) Mastogloia
sp. Scale bar =20 µm
okadaic acid and five isomers of DTX were detected from (Lucas et al., 1997). Recovered patients may experience the
samples collected from Johor Straits (Holmes et al., 1999). reactivation of ciguatera toxin from time to time (Lehane &
Two species of Dinophysis were detected from Singapore Lewis, 2000). Gambierdiscus yasumotoi was described from
in this study. They were D. caudata and D. rotundata Pulau Hantu, Singapore (Holmes, 1998). In this study, high
(Table 1; Fig. 1), with the former species associated with cell abundance of this toxic species was discovered in the
DSP (Marasigan et al., 2001). Two other species (D. ovum sediment samples from Pulau Hantu (Table 1; Fig. 1). Two
and D. sacculus) were reported previously from Singapore other undetermined species were also observed from the
(Pham et al., 2011). Five species were previously reported Singapore Strait. Gambierdiscus yasumotoi and G. belizeanus
from Malaysia (Usup et al., 2002c, Tan et al., 2013a). were also recorded from Malaysia (Leaw et al., 2011).
Gambierdiscus (Adachi & Fukuyo, 1979). This genus Gonyaulax (Diesing, 1866). Gonyaulax is a genus with
consists of 12 species, of which seven produce ciguatoxins 71 taxonomically accepted dinoflagellate species. Some
(CTX) and maitotoxins (MTX) (Parsons et al., 2012). members of this genus are known to possess yessotoxin,
Gambierdiscus spp. are known to cause ciguatera fish which can contaminate shellfish (Draisci et al., 1999, Rhodes
poisoning (Yasumoto et al., 1979). Toxins are transferred et al., 2006) and lead to diarrhetic shellfish poisoning (DSP).
to humans through consumption of contaminated reef fish Numerous studies have been conducted for G. spinifera, G.
(Holmes & Teo, 2002). Patients experience gastrointestinal polygramma and G. polyedra, all of which contain saxitoxin
uneasiness, cardiovascular and neurological signs and the (Bruno et al., 1990) and yessotoxin (Rhodes et al., 2006)
most profound symptom that differs from other forms of that can cause fish and shellfish mortality (Koizumi et al.,
seafood poisoning is the reversal of temperature sensation 1996, Draisci et al., 1999). Blooms of this species resulted
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Table 1. A checklist of marine dinoflagellates found in Singapore waters. The list is arranged alphabetically based on the scientific binominal
name, with the species authority and family as in AlgaeBase (Guiry & Guiry, 2014). * New record in Singapore.
in red discoloration of the sea, and this has been reported in Karenia (Hansen & Moestrup, 2000). This genus is currently
Malaysia (Lim et al., 2014b). Gonyaulax spinifera (Claparède known to comprise 12 species. Toxins can be released into
& Lachmann) Diesing 1866 was observed in the Singapore the environment as aerosols upon lysis of causative cells,
Strait for the first time in this study. causing humans to suffer respiratory problems (Ishida et
al., 1996; Pierce et al., 2004). Recreational beaches have
Heterocapsa (Stein, 1883). This dinoflagellate genus been forced to close due to blooms caused by members of
comprises 19 species. Blooms of Heterocapsa circularisquama this genus (Yang & Hodgkiss, 2004). Mortalities of fish,
resulted in mass mortality of commercially important echinoderms, polychaetes and bivalves are also associated
bivalves in Japan, such as the Pacific oyster, short-necked with such blooms (Yang & Hodgkiss, 2004, Silke et al.,
clam and blue mussel, incurring huge aquaculture losses 2005). Consumption of bivalves contaminated with this
(Matsuyama et al., 1997). Blooms cause bivalves to close genus may also result in neurotoxic shellfish poisoning
their shells, contract their mantle and eventually leading to (NSP) where patients experience headache, aching muscles,
death (Horiguchi, 1995, Matsuyama et al., 1996, Nagai et nausea, diarrhea and visual defects (Ishida et al., 1996).
al., 1996). In the South China Sea region, Hong Kong has Blooms of Karenia have been reported from Japanese and
experienced blooms of this species (Iwataki et al., 2002). Hong Kong waters in the western Pacific region (Yang &
One species, tentatively identified to Heterocapsa sp. 1, was Hodgkiss, 2004). An undetermined species was observed
found in Singapore. from the Singapore Strait in this study.
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Table 2. A checklist of marine diatoms found in Singapore waters. The list is arranged alphabetically based on scientific binominal name,
with species authority and family as in AlgaeBase (Guiry & Guiry, 2014). * new record in Singapore.
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230 Tryblionella cocconeiformis (Grunow) D.G.Mann in Round, Crawford & Mann 1990 Bacillariaceae
231 Tryblionella compressa (Bailey) M.Poulin in Poulin et al. 1990 Bacillariaceae
232 Tryblionella granulata (Grunow) D.G.Mann 1990 Bacillariaceae
233 Tryblioptychus cocconeiformis (Grunow) Hendey 1958 Surirellaceae
Karlodinium (Larsen, 2000). There are nine taxonomically also caused massive fish kills (P. minimum; Usup et al.,
accepted species in the genus Karlodinium (Daugbjerg et 2002c; Lim et al., 2012b).
al., 2000). They possess ichthyotoxins and karlotoxins (de
Salas et al., 2005, Adolf et al., 2009, Mooney et al., 2009, Nitzschia (Hassall, 1845). Nitzschia is a common genus of
Peng et al., 2010) that are known to cause massive fish kills diatoms in both freshwater and marine ecosystems. There
during blooms, significantly affecting aquaculture industries are some 423 valid species in this large genus. Species of
(Lim et al., 2014a). Karlodinium veneficum was first reported Nitzschia have not been responsible for any toxic blooms
from the Tebrau Strait in Malaysia (Tan et al., 2013a). In until 2000, when the first toxic Nitzschia, N. navis-varingica
February 2014, aquaculture finfishes amounting to some was reported to be responsible for a toxic bloom incident
50,000 individuals were killed. This was attributed to a in Vietnam (Lundholm & Moestrup, 2000). The toxin was
massive bloom of K. australe when cell densities reached confirmed as domoic acid (DA) which causes amnesic
1.25×106 cells L-1 in the Johor Strait, Malaysia (Lim et al., shellfish poisoning (ASP). Following that, a new toxigenic
2014a). In this survey, no cells resembling Karlodinium species, N. bizertensis was reported as a DA producer (Smida
spp. was detected. However, Karlodinium was found to be et al., 2014). There have been few studies of Nitzschia in
a common species in the Johor Straits (Lim et al., 2014a). the Southeast Asia region. Screening had been conducted by
Kotaki et al., 2006b in the region, and they reported toxic
Ostreopsis (Schmidt, 1901). There are nine taxonomically Nitzschia spp. in Thailand, Vietnam, Indonesia, Philippines
accepted species in this genus. Members of this benthic genus and Malaysia (Kotaki et al., 2006a, Romero et al., 2008,
possess palytoxins (PTX) and ovatoxins, which contaminate Romero et al., 2011, Romero et al., 2012, Thoha et al., 2012).
shellfish, crustaceans and several species of fish (Aligizaki At the same time there were some non-toxic strains isolated
et al., 2011). In 2005, around 200 people experienced from this region as well. In this study we identified some
respiratory symptoms when exposed to aerosols and 20 15 non-toxic species of Nitzschia from the Singapore Strait.
were hospitalized in Italy (Ciminiello et al., 2006; Tubaro
et al., 2011). Patients experience fever, sore throat, cough, Pseudo-nitzschia (Peragallo, 1900). Pseudo-nitzschia is a
nausea, vomiting and in some cases have caused fatalities cosmopolitan genus of diatoms, consisting of 45 valid species,
(Durando et al., 2007; Tubaro et al., 2011). When tested of which 16 are toxic. Recently, P. kodamae was shown to
on mice, these toxins cause blindness, numbness and death be the first toxic Pseudo-nitzschia species in Southeast Asia
(Aligizaki et al., 2011). Species from this genus have been (Teng et al., 2014). Dao et al. (2014) reported the presence
reported from Malaysia, Indonesia and Vietnam (Leaw et al., of toxic P. cf. caciantha from Vietnam. This species is
2001; Penna et al., 2012; Tan et al., 2013b). In this study, believed to be associated with domoic acid occurrences
one species (Ostreopsis ovata; see Table 1) was found in in the spiny oyster Spondylus versicolor in Vietnam (Dao
the Singapore Strait. et al., 2006; Dao et al., 2009; Ha et al., 2014). However,
no blooms of Pseudo-nitzschia associated with Amnesic
Prorocentrum (Ehrenberg, 1834). There are 82 taxonomically Shellfish Poisoning (ASP) were reported in Southeast Asia
accepted species in this dinoflagellate genus. Some species thus far. Some 30 Pseudo-nitzschia spp. are found in the
possess okadaic acid and pectentoxins (Murakami et al., region, with ten of them being potentially toxic (Priisholm
1982; Yasumoto et al., 1987; Lee et al., 1989; Zhou & Fritz, et al., 2002, Larsen and Nguyen-Ngoc, 2004, Bajarias et al.,
1994), which are associated with blooms (Pybus, 1990) that 2006, Yap-Dejeto et al., 2010, Lim et al., 2012a, Lim et al.,
may lead to ciguatera fish poisoning and diarrhetic shellfish 2013a, Teng et al., 2013, Teng et al., 2014). In this survey,
poisoning (DSP) (Faust, 1991; Jackson et al., 1993; Heredia- five Pseudo-nitzschia species were recorded in Singapore
Tapia et al., 2002). Some species can secrete diatom growth waters (Lim et al., 2013b).
inhibitory and other substances with ichthyotoxic as well
as hemolytic properties (Uchida, 1977; Yasumoto et al., CONCLUSIONS
1987). Four Prorocentrum species were observed in this
study (P. concavum, P. gracile, P. lima and P. micans) The biodiversity of marine phytoplankton is rich in
(Fig. 1; Table 1). One species, P. lima, is associated with Singapore waters. The risk of Singapore waters of having
DSP events (Bauder et al., 1996). Several species have been non-indigenous species is also high due to intense port
reported from Malaysia, including okadaic acid producers activities. The marine phytoplankton list should be updated
that affected shellfish industries (P. lima, P. rathymum; see frequently and monitoring agencies should be aware of the
Mohammad-Noor et al., 2007; Tan et al., 2012), and have bloom forming species as well as toxin producers, which
might affect public health and seafood industries.
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