Potentially harmful dinoflagellates (Dinophyceae) from the coast of Pakistan
Sonia Munir¹, Zaib-un-nisa Burhan¹, P J A Siddiqui¹ & Steve L Morton²
¹Centre of Excellence in Marine Biology, University of Karachi-75270, Pakistan; [email protected]
²NOAA, Marine Biotoxins Program, 219 Fort Johnson Road, Charleston, SC, 29412, USA.
Abstract
A bimonthly interval (May 2002-July 2003) plankton survey was initiated at two separate sites along the
Manora Channel, Karachi Pakistan. Using both light and electron microscopy a large number of
dinoflagellates was identified, most of them first records for the Northern Indian Ocean. Potentially harmful,
bloomforming non-toxic dinoflagellate genera include Prorocentrum (11 species), Ceratium (21),
Scrippsiella (2), Gyrodinium (2), Katodinium (1), Noctiluca (1), Gymnodinium (2) , Akashiwo (1) and
Gonyaulax (5). A number of known toxin producers were also observed during the sampling period
including the ichthyotoxic dinoflagellate Cochlodinium (1), the okadaic acid producing Dinophysis (8), and
the saxitoxin producing Alexandrium (3). A number of typically benthic dinoflagellates were also observed
including okadaic acid and hepatotoxin producing Prorocentrum (4) and the palytoxin producer Ostreopsis
(1).
Introduction
Harmful algal blooms (HABs) in coastal areas
often cause shellfish, finfish, mammal mortality,
and can damage aquaculture farms (Banner et al.
1960; Smayda 1990; Shumway 1990; Taylor
1993; Landsberg and Steidinger 1997; Richlen et
al. 2010). The occurrence of high biomass nontoxic dinoflagellates can initiate harmful algal
blooms, known as red tides, brown tides, green
tides (discoloration of water) and cause oxygen
depletion (Smayda 1990; Hallegraeff 1993;
Landsberg 2002), affecting the aquatic
environment. Phytoplankton studies are sporadic
along the Pakistan coastline. Previous plankton
surveys from the Arabian Sea have reported a
number of potential bloom forming species such
as Prorocentrum micans (Hassan and Saifullah
1971), Gonyaulax spp (Saifullah and Hassan
1973), Ceratium shurunk (Hassan and Saifullah
1974), Gonyaulax diesing (Chaghtai and Saifullah
2001) and Noctiluca scintillans (Chaghtai and
Saifullah 2006). This paper describes potentially
harmful dinoflagellates from the northern Arabian
Sea, Manora coast of Karachi, Pakistan.
Material and Methods
Triplicate samples were collected bimonthly
during May 2002-July 2003 from near shore
waters of Karachi harbor: St. I (24˚49.77'N
66˚57.85'E) and Mouth of Manora Channel St. II
(24˚47.93'N 66˚58.87'E) Karachi. Niskin bottle
samples were collected at 1m depth and fixed with
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Lugol. Cells were enumerated using the Utermohl
technique. For identification, epifluoresence
microscopy (BX 51, Olympus, Japan) and
scanning electron microscopy (JEOL, 5600Lv)
were used. The epifluoresence microscope was
equipped with a magnafire digital color camera
(Olympus, Tokyo, Japan), in order to examine
cells using differential interference contrast (DIC)
microscope. Cells were stained with 1%
calcofluor white MR2 (Sigma, St Louis, MO) to
visualize the thecal plates and thecate species
identification was done according to Kofoidian
plate tabulation. For scanning electron microscopy
(SEM), cells were desalted using a 10% step
gradient of seawater to freshwater and dehydrated
by using a series of acetone. After dehydration,
samples were coated with 1.5 nm of gold-platium
using a Denton sputter-edge coater (Moorestown,
NJ) and examined with a JEOL 5600LV (Tokyo,
Japan) scanning electron microscope.
Results
A total of 98 species were identified including 61
species which were first reports from Pakistani
waters. Among them 66 species were blooms
forming non-toxic harmful species including
Prorocentrum,
Ceratium,
Scrippsiella,
Gyrodinium,
Akashiwo,
Heterocapsa
cf.
circularisquama,
Katodinium,
Noctiluca,
Gymnodinium, and Protoperidinium (Table 1). A
total of 28 species were known toxin producing
dinoflagellates
including
Gymnodinium,
Gonyaulax,
Lingulodinium,
Dinophysis,
Alexandrium, and Cochlodinium. A number of
known toxic epiphytic dinoflagellates, including
the genus Prorocentum, and Ostreopsis, were also
observed in planktonic samples (Table 2). Our
results indicated that maximum cells densities per
litre of Alexandrium ostenfeldii, Prorocentrum
minimum, P. dongaiense, Scrippsiella trochoidea
was > 1000-6000 cells/L has great diversity
throughout the year and these were most dominant
species found from both stations (Tables 1 & 2).
Dinophysis
caudata,
Ceratium
furca,
Prorocentrum micans were frequent occurring
species (Tables 1 & 2) and number of toxic
species found rare from St. A for example,
Lingulodinium
polyedricum,
Protoceratium
reticulatum,
Gymnodinium
catenatum,
Alexandrium minutum, D. acuta, D. miles and D.
fortii, D. rotundata, D.infundibula etc from St. B
(Table 2).
Discussion
The coastal area of Karachi is influenced by
anthropogenic activities, whereas industrial,
agricultural and domestic waste from Layari river,
adversely influence water quality of Manora
Channel. During this survey a number of both
toxic and non-toxic dinoflagellates were recorded
along the coast of Pakistan, showing the potential
for future HAB events. A number of these nontoxic species such as Prorocentrum minimum, P.
donghiense, and Ceratium fusus have been linked
to coastal eutrophication worldwide. Due to the
presence of toxin producing dinoflagellates, the
coast of Pakistan is at risk from shellfish and
finfish toxic events from saxitoxin and okadaic
acid-like toxins, spirolides, yessotoxin, palytoxin,
hepatotoxin and ciguatoxin. Most of these toxic
species have not been observed in the northern
Arabian Sea previously. The morphological
characters of the toxic dinoflagellates have been
described (Fig 1). However additional studies are
required to determine if toxins are present in the
coastal area of Pakistan.
Acknowledgements
This research was supported by Higher Education
Commission, Islamabad Pakistan and scholarship
(International Research Support Initiative
Program) to SM to study in Charleston USA.
Fig. 1. Potentially toxic dinoflagellates from
Pakistan. A, B Alexandrium ostenfeldii; C. A.
minutum; D. A. tamarense; E-F. A. tamiyavanichi; G. Dinophysis caudata; H. D.miles; I.
D.acuminata; J. D.fortii; K. D. rotundata; L. D.
infundibulus; M. D.acuta; N. Gonyaulax
spinifera; O. G. polygramma; Q-R. G. verior; S.
Lingulodinium polyedricum; T. Protoceratium
reticulatum; U. Gymnodinium catenatum.
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References
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Table 1. Important red-tide species of dinoflagellates from St. A and St. B, Karachi coast ;
Dominant (*****), Abundant (****), Frequent (***), Rare (**, *).
Species
Akashiwo sanguinea
Ceratium furca
C. lineatum
C. fusus
Heterocapsa cf.
circularisquama
Prorocentrum micans
P. dongaiense
Scrippsiella trochoidea
Pyrophacus steinii
Protoperidinium divergens
St. A
**
*
*
*
St. B
**
**
**
***
Fishery impacts
Redtide
Fish killer, redtide
Fish killer, redtide
Fish killer, redtide
*
***
****
****
**
**
***
****
*****
****
***
**
Fish killer, redtide
Fish killer, redtide
Fish killer, redtide
Fish killer, redtide
Fish killer, redtide
Fish killer, redtide
Table 2. Potential toxin producing dinoflagellates from St. A and St. B, Pakistan
Dominant (*****), Abundant (****), Frequent (***) and Rare (**,*)
Species
Alexandrium concavum
A. ostenfeldii
A.tamarense
A. tamiyavanichi
A. minutum
Cochlodinium cf. fulvescens
Dinophysis acuminata
D. acuta
D. caudata
D. fortii
D. rotundata
D.infundibula
D. miles
D. mitra
Gymnodinium catenatum
Gonyaulax spinifera
G. digitalis
G. polygramma
G. verior
Ostreopsis cf ovata
Protoceratium reticulatum
Lingulodinium polyedricum
Prorocentrum balticum
P. faustiae
P. lima
P. minimum
St. A
*
****
***
**
*
**
*
*
**
Absent
Absent
Absent
*
*
*
**
*
*
*
*
*
*
**
*
*
****
St. B
Absent
*****
Absent
**
Absent
***
*
Absent
**
*
*
*
Absent
Absent
Absent
***
**
Absent
*
**
Absent
Absent
**
Absent
Absent
*****
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Toxins
Saxitoxin and Congeners
Saxitoxin and/or spirolides (some strains)
Saxitoxin and Congeners
Saxitoxin and Congeners
Saxitoxin and Congeners
Unidentified icthyotoxic
Okadaic acid and congeners
Okadaic acid and congeners
Okadaic acid and congeners
Okadaic acid and congeners
Okadaic acid and congeners
Okadaic acid and congeners
Okadaic acid and congeners
Okadaic acid and congeners
Saxitoxin and Congeners
Yessotoxins (some strains only)
Yessotoxins (some strains only)
Yessotoxins (some strains only)
Yessotoxins (some strains only)
Palytoxin like compound
Yessotoxins
Homoyessotoxins
Unidentified hepatotoxins (some strains)
Okadaic acid and congeners
Okadaic acid and congeners
Unidentified hepatotoxins (some strains)