Post on 21-Feb-2023
Environ Monit AssessDOI 10.1007/s10661-010-1855-z
Dinoflagellate community structure from the stratifiedenvironment of the Bay of Bengal, with special emphasison harmful algal bloom species
Ravidas Krishna Naik · Sahana Hegde ·Arga Chandrashekar Anil
Received: 29 June 2010 / Accepted: 19 December 2010© Springer Science+Business Media B.V. 2011
Abstract Harmful algal blooms (HABs) havebeen documented along the coasts of India andthe ill effects felt by society at large. Most of thesereports are from the Arabian Sea, west coast ofIndia, whereas its counterpart, the Bay of Bengal(BOB), has remained unexplored in this context.The unique characteristic features of the BOB,such as large amount of riverine fresh water dis-charges, monsoonal clouds, rainfall, and weak sur-face winds make the area strongly stratified. Inthis study, 19 potentially harmful species whichaccounted for approximately 14% of the totalidentified species (134) of dinoflagellates wereencountered in surface waters of the BOB duringNovember 2003 to September 2006. The varia-tions in species abundance could be attributedto the seasonal variations in the stratificationobserved in the BOB. The presence of fre-quently occurring HAB species in low abundance(≤40 cell L−1) in stratified waters of the BOB maynot be a growth issue. However, they may play asignificant role in the development of pelagic seedbanks, which can serve as inocula for blooms ifcoupled with local physical processes like eddies
R. K. Naik · S. Hegde · A. C. Anil (B)National Institute of Oceanography,Council of Scientific and Industrial Research,Dona Paula, Goa, 403004, Indiae-mail: acanil@nio.org
and cyclones. The predominance of Ceratiumfurca and Noctiluca scintillans, frequently occur-ring HAB species during cyclone-prone seasons,point out their candidature for HABs.
Keywords Ceratium furca · Noctiluca scintillans ·Bay of Bengal · Stratification · Cyclones · Eddies
Introduction
Harmful algal blooms (HABs) are natural phe-nomena; historical records indicate their occur-rence long before the advent of human activitiesin coastal ecosystems. Recent surveys have dem-onstrated a dramatic increase and geographicspread in HAB events in the last few decades(Anderson 1989; Smayda 1990; Hallegraeff 1993).Thus, knowledge of the present geographic distri-bution and seasonal fluctuations in HAB species isimportant to understand globally spreading HABevents (GEOHAB 2001). In fact, Hallegraeff(2010) has reported that unpreparedness for suchsignificant range expansions or spreading of HABproblems in poorly monitored areas will be oneof the greatest problems for human society in thefuture.
Among the total marine phytoplankton species,approximately 7% are capable of forming algalblooms (red tides; Sournia 1995); dinoflagellates
Environ Monit Assess
are the most significant group producing toxicand harmful algal blooms (Steidinger 1983, 1993;Anderson 1989; Hallegraeff 1993) accounting for75% of the total HAB species (Smayda 1997).
Blooms result from a coupling mechanism in-volving physical, chemical, and biological factors.Though dynamics of blooms is complex, the roleor mechanism of chemical and biological factorsare now reasonably understood (Fistarol et al.2004; Solé et al. 2006; GEOHAB 2006; Adolf et al.2007; Waggett et al. 2008). However, comparableunderstanding about physical factors is lackingexcept for few examples (Maclean 1989; Karl et al.1997; Belgrano et al. 1999; Yin et al. 1999). Im-pacts of these factors in combination with localinter-annual meteorological conditions will varyfrom one geographical location to the other andwill thus influence bloom dynamics differentially.
HAB studies in Indian waters indicate reason-able reports on HABs and their impacts alongthe west coast of India. Direct impacts of HABson human health have also been reported fromMangalore (Karunasagar et al. 1984); they relatedthe death of a boy to an outbreak of paralyticshellfish poisoning (PSP) following consumptionof clams. Dinoflagellate toxins have also beenrecorded in shellfish from surrounding estuariesnear Mangalore in 1985 and 1986 (Segar et al.1989). Planktonic and cyst forms of Gymnodiniumcatenatum, a PSP-producing dinoflagellate fromthis region were detected later on (Godhe et al.1996) and the importance of close monitoringof coastal waters, sediment, and shellfish washighlighted.
Compared to the above regions, the Bay ofBengal (BOB), the eastern arm of the Indian
AndamanSea
PK transect
CP transect
12 3 4 5 6 7
8 9 10 11 12 13
1415
16
17
18
19
20
21
22
75° 80° 85° 90° 95°Longitude
E
N
10°
5°
20°
15°
Lat
itude
Fig. 1 Study area map showing station locations along the Chennai–Port Blair (CP) and Port Blair–Kolkata (PK) transectsin the Bay of Bengal
Environ Monit Assess
Ocean, remains relatively unexplored in the con-text of HAB studies. The BOB is known for itsunique characteristic features: large volume offreshwater input from river discharge and rainfall,warmer sea surface temperatures, monsoonalclouds and reversal of currents. The riverine in-put into this area injects loads of nutrients andsuspended sediment in the BOB (Gordon et al.2002; Mukhopadhyay et al. 2006). These featurespoint to the suitability of the BOB as a zone pronefor algal blooms including HAB events. However,the strongly stratified surface layer of the BOBrestricts the transport of nutrients from deeperlayers to the surface (Prasanna Kumar et al. 2002).Thus, it is very interesting to understand theseasonal variations in dinoflagellate communitystructure in this inimitable geographic region.
Since taking oceanic cruises on regular intervalsis not cost-effective, the “ships of opportunity”program, supported by the Indian ExpendableBathythermograph (XBT) project, was used.Therefore, the present study on the spatial andtemporal distribution of dinoflagellates in theBOB, with emphasis on HAB species, is the firstof its kind from the region. The following objec-tives were addressed: (1) dinoflagellate distribu-tion in the surface waters of the BOB and (2)detailing of the HAB species present and theirseasonal occurrence.
Materials and methods
Study area and sampling
This study was conducted with the support of theXBT program. Surface water samples were col-lected using steel buckets from the moving ship.This method was selected in order to minimize thephysical damage to cells compared to the methodof collecting samples using a pump. The sampleswere collected on two transects [Chennai to PortBlair (CP, 12 stations) and Port Blair to Kolkata(PK, 10 stations)] (Fig. 1), from passenger shipsplying along these transects. Samples were col-lected at one-degree intervals along both transect,from November 2003 to September 2006 coveringdifferent seasons. Among the sampling stationsfrom CP (central BOB) and PK (northern BOB)
Table 1 Station details of Chennai–Port Blair (CP) andPort Blair–Kolkata (PK) transects
Stations Lat (N) Long (E)
CP transect1 13.04 81.072 13.09 82.033 13.09 834 13.04 84.055 13.05 85.056 12.49 867 12.38 878 12.23 88.039 12.1 8910 11.52 90.0511 11.41 91.0412a 11.28 92.07
PK transect13a 12.03 93.1414a 13.01 93.1415 14 92.5616 15.01 92.2417 16.08 91.2918 17.09 90.4319 18 90.1220 19 89.321 20 88.522a 21.05 88.14
aNear coastal stations
transects, the majority were oceanic whereas, fewstations are near the coast (Table 1). Samples(1 L) were fixed with Lugol’s iodine solution forthe laboratory enumeration and identification ofdinoflagellates to the lowest possible taxonomiclevel.
Microscopic analysis
The 1-L sample was kept settling for 48 h. Afterthat, the volume was brought down to 100 ml andthen to 10 ml final concentration after another48-h settling period (method modified from Hasle1978). From this 10-ml final concentration, 3 mlconcentrated sample was taken in a petri dish(3.8 cm diameter) and examined under an Olym-pus inverted microscope at ×100 to ×400 mag-nification. Identification of the dinoflagellate taxawas carried out using the keys provided bySubrahmanyan (1968), Taylor (1976), Tomas(1997), Horner (2002), and Hallegraeff et al.(2003).
Environ Monit Assess
Tab
le2
Tax
onom
iclis
tofi
dent
ifie
ddi
nofl
agel
late
sdu
ring
the
stud
ype
riod
alon
gth
eC
Pan
dP
Ktr
anse
cts
(*po
tent
ially
HA
Bsp
ecie
s,†
new
repo
rtin
g)
CP
tran
sect
PK
tran
sect
Feb
04Ju
n04
Jul0
4O
ct04
Sep0
6N
ov03
Mar
04A
ug04
Oct
04Se
p06
Aut
otro
phic
dino
flag
ella
tes
Ale
xand
rium
conc
avum
0–2
(1)
Ale
xand
rium
spp.
0–2
(2)
0–9
(1)
0–2
(1)
0–20
(1)
0–6
(1)
Am
phid
iniu
msp
.*0–
7(5
)0–
2(1
)0–
2(1
)0–
5(3
)0–
12(1
0)0–
8(2
)0–
5(1
)0–
9(8
)A
mph
isol
enia
bide
ntat
a0–
2(2
)0–
8(7
)0–
3(1
)0–
3(3
)0–
2(1
)0–
9(3
)A
mph
isol
enia
glob
ifer
a0–
3(2
)B
leph
aroc
ysta
sp.
0–4
(2)
0–4
(3)
0–8
(2)
0–4
(5)
0–8
(6)
0–3
(1)
Cer
atoc
orys
arm
ata
0–2
(1)
0–2
(1)
Cer
atoc
orys
horr
ida
0–4
(2)
0–3
(1)
0–2
(2)
Cor
ytho
dini
umco
nstr
ictu
m0–
2(1
)0–
4(2
)C
oryt
hodi
nium
eleg
ans
0–4
(1)
0–3
(1)
0–3
(1)
0–3
(1)
Cor
ytho
dini
umm
icha
elsa
rsi
0–8
(2)
Cor
ytho
dini
umre
ticul
atum
0–2
(2)
0–2
(2)
Cor
ytho
dini
umte
ssel
atum
0–2
(2)
0–2
(1)
0–3
(2)
0–3
(3)
0–2
(2)
0–3
(2)
Cor
ytho
dini
umsp
.0–
2(1
)0–
3(1
)E
nsic
ulif
era
sp.
0–5
(1)
Gam
bier
disc
ussp
.*†
0–4
(1)
Gon
iodo
ma
poly
edri
cum
0–2
(2)
0–6
(2)
0–2
(1)
0–5
(1)
Gon
iodo
ma
spha
eric
um0–
6(3
)0–
3(1
)0–
6(1
)0–
2(2
)0–
5(1
)0–
3(2
)G
onya
ulax
brev
isul
cata
0–3
(1)
Gon
yaul
axdi
gita
lis0–
5(1
)G
onya
ulax
grin
dley
i0–
2(1
)G
onya
ulax
mon
ospi
na†
0–3
(1)
0–3
(1)
Gon
yaul
axpo
lyed
ra*
0–4
(4)
0–3
(1)
0–2
(1)
Gon
yaul
axpo
lygr
amm
a*0–
8(1
)0–
2(1
)0–
2(1
)0–
8(4
)0–
6(1
)0–
4(2
)0–
4(1
)0–
4(2
)0–
8(3
)0–
6(2
)G
onya
ulax
scri
ppsa
e0–
4(1
)0–
2(2
)0–
3(1
)0–
6(3
)G
onya
ulax
spin
ifer
a*0–
4(4
)0–
3(1
)0–
4(1
)0–
2(2
)G
onya
ulax
sp.
0–2
(1)
0–2
(2)
0–2
(2)
0–3
(1)
0–6
(6)
0–2
(1)
0–4
(2)
0–6
(1)
0–3
(2)
0–3
(5)
Gym
nodi
nium
spp.
*0–
2(1
)0–
5(1
)0–
6(3
)0–
6(1
)0–
6(3
)O
xyto
xum
glob
osum
0–26
(1)
Oxy
toxu
mla
ticep
s0–
3(1
)0–
6(3
)0–
2(1
)0–
6(4
)O
xyto
xum
scol
opax
0–3
(5)
0–2
(2)
0–4
(6)
0–8
(4)
0–3
(5)
0–6
(2)
0–2
(2)
0–5
(1)
0–3
(4)
Oxy
toxu
msc
eptr
um0–
2(1
)0–
4(5
)0–
3(4
)0–
2(3
)0–
3(1
)O
xyto
xum
sp.
0–6
(3)
0–2
(1)
0–2
(2)
0–3
(1)
Environ Monit Assess
Pod
olam
pas
bipe
s0–
2(3
)0–
3(1
)0–
3(2
)0–
2(1
)0–
5(1
)0–
6(2
)P
odol
ampa
sel
egan
s0–
4(3
)0–
2(1
)P
odol
ampa
spa
lmip
es0–
4(4
)0–
2(2
)0–
2(3
)0–
3(3
)0–
6(1
)0–
2(1
)0–
2(1
)0–
5(1
)0–
3(1
)P
odol
ampa
ssp
inif
era
0–2
(1)
0–2
(2)
0–3
(1)
0–5
(1)
Pyr
opha
cus
stei
nii
0–2
(1)
0–3
(1)
0–2
(3)
0–2
(1)
0–18
(1)
Pyr
opha
cus
spp.
0–5
(2)
Tor
odin
ium
tere
do†
0–3
(2)
Mix
otro
phic
dino
flag
ella
tes
Ale
xand
rium
min
utum
*0–
10(1
)C
erat
ium
arie
tinum
0–3
(2)
Cer
atiu
maz
oric
um0–
3(1
)0–
2(1
)C
erat
ium
cand
elab
rum
f.de
pres
sum
0–2
(1)
0–3
(1)
0–3
(1)
Cer
atiu
mco
ntor
tum
0–5
(3)
0–4
(1)
Cer
atiu
mde
clin
atum
0–2
(1)
0–2
(1)
0–5
(4)
0–9
(4)
0–5
(1)
0–9
(3)
Cer
atiu
mde
flex
um0–
3(1
)0–
8(1
)C
erat
ium
dens
0–3
(1)
Cer
atiu
mex
tens
um0–
4(4
)0–
6(1
)C
erat
ium
furc
a*0–
2(1
)0–
2(2
)0–
5(4
)0–
9(5
)0–
20(5
)0–
6(4
)0–
13(4
)0–
18(4
)C
erat
ium
fusu
s*0–
6(4
)0–
2(4
)0–
2(3
)0–
13(9
)0–
6(4
)0–
20(1
)0–
4(1
)0–
6(5
)0–
8(7
)0–
12(3
)C
erat
ium
gibb
erum
0–2
(1)
Cer
atiu
mho
rrid
um0–
2(2
)0–
6(2
)0–
2(1
)0–
3(1
)C
erat
ium
kars
teni
i0–
2(4
)0–
2(1
)C
erat
ium
kofo
idii
0–2
(1)
0–2
(1)
0–2
(1)
Cer
atiu
mlin
eatu
m0–
2(2
)0–
3(2
)0–
3(1
)0–
5(1
)0–
3(1
)C
erat
ium
lunu
la0–
2(1
)C
erat
ium
mac
roce
ros
0–2
(3)
0–2
(1)
0–2
(3)
0–2
(1)
Cer
atiu
mpe
ntag
onum
0–9
(7)
0–2
(1)
0–3
(1)
Cer
atiu
msc
hmid
tii0–
2(2
)0–
5(3
)0–
3(1
)0–
8(2
)C
erat
ium
sym
met
ricu
m0–
10(4
)0–
3(1
)0–
2(2
)C
erat
ium
tere
s0–
8(6
)0–
8(7
)0–
8(7
)0–
9(7
)0–
4(1
)0–
2(1
)0–
3(2
)0–
12(3
)C
erat
ium
tric
hoce
ros
0–2
(2)
0–8
(1)
Cer
atiu
mtr
ipos
0–2
(1)
0–2
(1)
0–2
(1)
Cer
atiu
mvu
ltur
0–4
(1)
0–3
(1)
Cer
atiu
msp
p.0–
2(1
)0–
3(2
)0–
3(3
)0–
5(1
)D
inop
hysi
sca
udat
a*0–
2(1
)0–
5(1
)D
inop
hysi
sm
iles*
0–12
(1)
Din
ophy
sis
schu
ettii
0–3
(1)
Din
ophy
sis
spp.
0–4
(5)
0–2
(2)
0–5
(2)
0–6
(6)
0–5
(1)
0–3
(1)
Dis
sodi
umas
ymm
etri
cum
0–2
(1)
Environ Monit Assess
Tab
le2
(con
tinu
ed)
CP
tran
sect
PK
tran
sect
Feb
04Ju
n04
Jul0
4O
ct04
Sep0
6N
ov03
Mar
04A
ug04
Oct
04Se
p06
Pro
roce
ntru
mar
cuat
um†
0–2
(1)
0–4
(1)
Pro
roce
ntru
mbe
lizea
num
*†
0–24
(1)
Pro
roce
ntru
mco
mpr
essu
m0–
2(1
)0–
5(1
)0–
2(1
)P
roro
cent
rum
grac
ile0–
8(4
)P
roro
cent
rum
lent
icul
atum
0–4
(1)
Pro
roce
ntru
mlim
a*0–
2(1
)P
roro
cent
rum
mic
ans*
0–20
(1)
0–2
(2)
0–3
(1)
0–3
(2)
0–10
(1)
0–10
(2)
0–9
(1)
Pro
roce
ntru
mm
inim
us*
0–2
(1)
0–2
(1)
0–3
(1)
0–2
(1)
Pro
roce
ntru
mm
exic
anum
*0–
5(6
)P
roro
cent
rum
obtu
sum
0–8
(3)
0–3
(2)
0–3
(2)
Pro
roce
ntru
msc
utel
lum
†0–
2(1
)P
roro
cent
rum
sigm
oide
s*0–
2(1
)0–
3(1
)0–
9(4
)P
roro
cent
rum
sp.
0–2
(2)
0–14
(2)
0–4
(3)
0–8
(5)
0–9
(7)
0–4
(4)
0–4
(1)
0–6
(2)
0–8
(3)
0–6
(5)
Pyr
ocys
tisfu
sifo
rmis
0–2
(1)
0–3
(1)
Pyr
ocys
tisha
mul
us0–
2(1
)0–
4(2
)0–
2(1
)P
yroc
ystis
lunu
la0–
4(1
)P
yroc
ystis
spp.
0–2
(1)
0–2
(1)
0–3
(1)
0–3
(2)
0–14
(5)
0–6
(1)
0–5
(2)
0–3
(1)
Scri
ppsi
ella
troc
hoid
ea*
0–14
(9)
0–2
(1)
0–3
(1)
0–9
(7)
0–26
(6)
0–4
(1)
0–5
(2)
0–15
(7)
Scri
ppsi
ella
spp.
0–2
(1)
0–6
(5)
0–10
(3)
0–2
(1)
0–6
(3)
0–8
(1)
Het
erot
roph
icdi
nofl
agel
late
sG
otoi
usab
ei†
0–6
(4)
0–3
(1)
0–10
(5)
0–8
(4)
0–3
(1)
His
tione
isca
rina
ta†
0–2
(1)
0–3
(1)
0–4
(2)
His
tione
isco
stat
a†
0–2
(1)
0–2
(1)
0–2
(1)
His
tione
isde
pres
sa0–
2(2
)0–
2(2
)H
istio
neis
spp.
0–3
(1)
Kat
odin
ium
sp.
0–2
(3)
0–4
(5)
0–10
(2)
0–3
(2)
0–2
(2)
0–5
(1)
Noc
tiluc
asc
intil
lans
0–2
(1)
0–40
(1)
0–2
(1)
Noc
tiluc
asp
p.0–
2(1
)O
rnith
ocer
cus
hete
ropo
rus
0–6
(2)
0–2
(1)
Orn
ithoc
ercu
sm
agni
ficu
s0–
2(2
)0–
4(2
)0–
18(2
)0–
3(1
)0–
5(1
)0–
6(2
)O
rnith
ocer
cus
quad
ratu
s0–
2(1
)0–
2(1
)0–
3(1
)0–
5(1
)O
rnith
ocer
cus
stei
nii
0–2
(1)
0–4
(2)
0–2
(1)
0–2
(1)
0–5
(1)
Orn
ithoc
ercu
sth
umii
0–2
(1)
0–4
(2)
0–2
(1)
0–5
(1)
Environ Monit Assess
Orn
ithoc
ercu
ssp
p.0–
2(1
)0–
3(1
)O
xyph
ysis
spp.
0–3
(1)
Pen
taph
arso
dini
umsp
.†0–
2(1
)0–
4(1
)P
hala
crom
aar
gus
0–2
(1)
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lacr
oma
cune
us0–
2(1
)0–
5(1
)P
hala
crom
ara
pa0–
2(2
)0–
2(1
)0–
3(1
)P
hala
crom
aro
tund
atum
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(1)
0–2
(1)
0–8
(2)
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(2)
Pha
lacr
oma
spp.
0–2
(2)
0–2
(2)
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(1)
Pro
noct
iluca
pela
gica
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noct
ulic
asp
inif
era
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(2)
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Pro
tope
ridi
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met
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m0–
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es0–
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)P
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dini
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asip
es*
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(1)
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tope
ridi
nium
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essu
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(6)
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(5)
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tope
ridi
nium
eleg
ans
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(2)
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tope
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nium
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de0–
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)P
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peri
dini
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tope
ridi
nium
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tope
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nium
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ngum
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um0–
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)P
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dum
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tope
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ncul
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rme
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tope
ridi
nium
sp.
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abik
odin
ium
sp.
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The
valu
esou
tsid
ebr
acke
tin
dica
teth
era
nge
ofab
unda
nce
duri
ngth
atm
onth
and
valu
esin
side
the
brac
ket
indi
cate
sth
efr
eque
ncy
ofoc
curr
ence
atC
P(t
otal
12st
atio
ns)
and
PK
(tot
al10
stat
ions
)tr
anse
cts
duri
ngth
ere
spec
tive
sam
plin
gm
onth
s
Environ Monit Assess
Data analyses
To evaluate seasonal differences, the observa-tional period was classified into three seasons:Pre-monsoon (PrM—February to March 04),South west monsoon (SWM—June 04, July 04,August 04, September 06) and Post-monsoon(PoM—November 03, October 04).
Univariate measures [Shannon–Wiener diver-sity index (H′), Margalef’s species richness (d)and Pielou’s evenness (J′)] were analyzed usingPRIMER (version 5, developed by PRIMER-ELimited, UK) and the variations in thesewere determined by two-way ANOVA. Two-way ANOVA was also performed on thedinoflagellate abundance data to evaluate spatialand temporal variation (Sokal and Rohlf 1981).Spatial variation in the dinoflagellate communityand the abundance profiles of the five mostdominant taxa during each sampling period in
both transects are presented as SURFER plotsusing the SURFER 8 program (developed byGolden Software Inc., USA). The percentagecontribution of autotrophic, mixotrophic, andheterotrophic forms of dinoflagellates in eachsampling period was also calculated.
Results
Taxonomic identification revealed 134 species ofdinoflagellates in surface waters of the BOB dur-ing the observation period (Table 2). Furthergrouping of these identified species based ontheir nutritional mode, revealed 40 autotrophic,50 mixotrophic, and 44 heterotrophic species,indicated the dominance of mixotrophic forms(Table 2). Comparison of this report with earlierreported species from the same area (Taylor 1976;Jyothibabu et al. 2003; Paul et al. 2007) indicated
Longitude Longitude Longitude
Lat
itude
N
E
Lat
itude
(b) (c)
13
14
15
16
17
18
19
20
21
22
10
12
14
16
18
20
22
10
12
14
16
18
20
22
15
16
17
18
19
20
22
21
14
13
1 2 3 4 56 7 8 9
10 11 12
INDIAINDIA
INDIA
1 2 3 4 56 7 8 9
10 11 12
80 82 84 86 88 90 92 94 80 82 84 86 88 90 92 94 80 82 84 86 88 90 92 94
15
16
17
18
19
20
22
21
14
13
1 2 4 56 7 8 9
10 11 12
3
15
16
17
18
19
20
22
21
14
13
1 2 3 4 56 7 8 9
10 11 12
15
16
17
18
19
20
22
21
14
13
1 2 3 4 56 7 8 9
10 11 12
0
10
20
30
40
50
60
70
80
90
100
(a) (b) (c)
(f)(e)(d)
Fig. 2 Spatio-temporal variation in total dinoflagellate abundance (cell L−1) along the Chennai–Port Blair (CP) and PortBlair–Kolkata (PK) transects in a Nov 03, b Feb–Mar 04, c Jun 04, d Jul–Aug 04, e Oct 04 and f Sep 06
Environ Monit Assess
Tab
le3
Tw
o-w
ayA
NO
VA
toev
alua
teth
eva
riat
ion
into
tald
inof
lage
llate
abun
danc
e,sp
ecie
sri
chne
ss,e
venn
ess,
and
dive
rsit
yal
ong
the
CP
and
PK
tran
sect
s
CP
tran
sect
PK
tran
sect
dfSS
MS
Fs
Pva
lue
dfSS
MS
Fs
Pva
lue
Abu
ndan
ceSt
atio
ns11
3319
302
10.
2817
930
9234
41
0.49
43Se
ason
s4
5025
1256
50.
0016
434
9387
32
0.06
63W
ithi
nsu
b-gr
oup
erro
r44
1057
624
036
1299
436
1T
otal
5918
920
4919
579
Spec
ies
even
ness
Stat
ions
100
01
0.19
229
00
10.
2578
Seas
ons
40
01
0.31
454
00
20.
0710
Wit
hin
sub-
grou
per
ror
400
036
10
Tot
al54
049
1Sp
ecie
sri
chne
ssSt
atio
ns10
101
20.
1661
910
13
0.01
80Se
ason
s4
00
00.
9585
43
12
0.16
14W
ithi
nsu
b-gr
oup
erro
r40
271
3614
0T
otal
5437
4927
Spec
ies
dive
rsit
ySt
atio
ns10
30
20.
1033
94
02
0.03
38Se
ason
s4
10
10.
4078
42
03
0.04
83W
ithi
nsu
b-gr
oup
erro
r40
60
366
0T
otal
549
4912
Environ Monit Assess
ten new dinoflagellate species (Table 2 speciesmarked with †). Approximately 14% of the iden-tified species were potential HAB species (Table 2species marked with *).
Spatial and temporal distributionof dinoflagellate assemblages
The abundance of dinoflagellates ranged from0–94 cell L−1 throughout the observation periodat both CP and PK transects (Fig. 2). Thoughseasonal variation in dinoflagellate abundancewas observed in both transects, the variation wasstatistically significant at only the CP transect(Table 3). The highest average abundance ofdinoflagellates was observed during September06 (48 cell L−1 at PK) followed by October 04(40 cell L−1 at CP) whereas low abundance wasrecorded during June (21 cell L−1 at CP) andAugust 04 (22 cell L−1 at PK; Fig. 2). The spatialvariation in dinoflagellate abundance was not sta-tistically significant in both transects (Table 3).Species richness and diversity varied significantlyin the PK transect; species richness only acrossstations and diversity across both stations and sea-sons (Table 3). Mixotrophic dinoflagellates dom-inated across both transects, with the exceptionof October 04 at CP and September 06 at PKtransects, that were dominated by heterotrophicforms (Fig. 3). Ceratium was the dominant genusamong the mixotrophic forms whereas Protoperi-dinium was the dominant heterotrophic form.Ceratium fusus, Ceratium teres, Gotoius abei, Oxy-toxum scolopax, Protoperidinium ovatum, andScrippsiella trochoidea were among the abundantforms in both the transects. Amphisolenia biden-tata, Ceratium pentagonum, Ceratium symmet-ricum, Oxytoxum globosum, and Prorocentrumbelizianum were abundant only in CP transect(Fig. 4a) whereas Ceratium extensum, Ceratiumfurca, Dinophysis miles and Noctiluca scintillanswere abundant only in the PK transect (Fig. 4b).
Seasonal variation in HAB species
Overall, 19 potentially HAB species were encoun-tered in this area (Table 2). Some HAB specieswere present during all the seasons throughout the
37
48
15
26
45
29
35
38
27
22
35
43
35
46
18
4146
13
27
42
32
25
38
37
18
51
31
28
23
49
Autotrophic Mixotrophic Heterotrophic
(a)
(b)
(c)
(d)
(e)
(f)
(g)
(h)
(i)
(j)
Nov 03
Feb-Mar 04
Jun 04
Jul-Aug 04
Oct 04
Sep 06
CP transect PK transect
Fig. 3 The percentage contribution of autotrophic,mixotrophic and heterotrophic dinoflagellates along thea–e Chennai–Port Blair (CP) and f–j Port Blair–Kolkata(PK) transects. a Feb 04, b Jun 04, c Jul 04, d Oct 04, e Sep06, f Nov 03, g Mar 04, h Aug 04, i Oct 04 and j Sep 06
study period. These frequently occurring specieswere C. furca, C. fusus, Dinophysis sp., Gonyaulaxpolygramma, Gonyaulax sp., N. scintillans, Pro-rocentrum sp., S. trochoidea, Scrippsiella sp.(Table 2). Season-specific trends were also ob-served. Alexandrium minutum, Prorocentrum
Environ Monit Assess
Fig. 4 The five mostabundant species duringeach sampling period atthe (a) Chennai–PortBlair and (b) PortBlair–Kolkata transects.The maximum diameterof circle corresponds toaverage 9 cell L−1
b)
Feb04
Jun04
Jul04
Oct04
Sep06
Am
phis
olen
ia b
iden
tata
Am
phid
iniu
m s
p.
Cer
atiu
m fu
sus
Cer
atiu
m p
enta
gonu
m
Cer
atiu
m s
ymm
etri
cum
Cer
atiu
m te
res
Got
oius
abe
i
Oxy
toxu
m g
lobo
sum
Oxy
toxu
m s
colo
pax
Pro
roce
ntru
m b
eliz
ianu
m
Pro
roce
ntru
m s
p.
Pro
tope
ridi
nium
ova
tum
Pro
tope
ridi
nium
ped
uncu
latu
m
Pro
tope
ridi
nium
sp.
Scri
ppsi
ella
spp
.
Scri
ppsi
ella
troc
hoid
ea
a)
Oct04
Aug04
Mar04
Nov03
Sep06
Ale
xand
rium
spp
.
Am
phid
iniu
m s
p.
Ble
phar
ocys
ta s
p.
Cer
atiu
m e
xten
sum
Cer
atiu
m fu
rca
Cer
atiu
m fu
sus
Cer
atiu
m te
res
Din
ophy
sis
mil
es
Din
ophy
sis
spp.
Pyr
ocys
tis
spp
.
Got
oius
abe
i
Noc
tilu
ca s
cint
illa
ns
Oxy
toxu
m s
colo
pax
Pro
tope
ridi
nium
ova
tum
Pro
tope
ridi
nium
sp.
Scri
ppsi
ella
spp
.
Scri
ppsi
ella
troc
hoid
ea
lima, and Protoperidinium crassipes occurred onlyduring PrM whereas Dinophysis caudata, D. miles,Prorocentrum micans, P. mexicanum, P. minimus,Gymnodinium sp. and Gambierdiscus sp. werefound during SWM and PoM periods. Gonyaulaxpolyedra and G. spinifera occurred in PrM andPoM but not during SWM. In contrast to this, P.belizianum and P. sigmoides occurred only duringthe SWM.
Discussion
The BOB is a semi-enclosed tropical basin, distin-guished by a strongly stratified surface layer and
a seasonally reversing circulation (Shetye et al.1996). It is also influenced by monsoonal windsand enormous freshwater influx. The surfacestratified water column of the BOB restricts thevertical transport of nutrients from the bottomlayers to the surface, and therefore phytoplank-ton productivity as well (Prasanna Kumar et al.2002). The stratification is especially intense dur-ing the SWM period (Prasanna Kumar et al.2004) due to the influx of freshwater throughprecipitation and riverine discharges. The averageannual riverine discharge varies from the north-ern to southern bay with maximum discharge atnorth (1012 m3 from Ganges and Brahmaputra),medium at central (8.5 × 1010 m3 from Krishna
Environ Monit Assess
and Godavari) and minimum at southern bay(UNESCO 1988) resulting in variation in sur-face water salinity. Our study revealed that di-noflagellate abundance in surface waters wasgenerally in the range of 0–94 cell L−1 and didnot vary significantly across stations (Table 3).This could be related to the environmental condi-tions of the study area. Stratified water columns,with their characteristic oligotrophic conditions,tend to promote stasis of the resident popula-tion, rather than promoting growth or blooms(Smayda 2002). In fact, many studies (McGill1973; Paul et al. 2008) have reported that thesurface waters of the BOB are nitrate-deficient.Low surface PO3−
4 -P values of 0.1 μg-at L−1
have also been recorded in the Bay of Bengaland Andaman Sea (Kabanova 1964; Rozanov1964). Though the stratified BOB environmentsupported a rather homogeneous dinoflagellatecommunity in surface waters, significant seasonalvariations in abundance and species diversityof the dinoflagellate community were observed(Table 3). Minimum values were observed dur-ing SWM, correlating to the intensification of thestratified layer, and maximum during the with-drawal of the SWM and PoM (Fig. 2).
The dominance of mixotrophic dinoflagellatesin the study area could be a consequence ofthe prevalent low light and/or nutrient scarcity,conditions that are known to promote mixotro-phy (Legrand et al. 1998; Stoecker et al. 2006).Ceratium and Protoperidinium were the mostabundant representatives of the mixotrophic andheterotrophic forms in the BOB respectively(Fig. 4); their unique characteristics of verticalmigration, and heterotrophy are reasonably wellunderstood (Baek et al. 2006, 2007; Baek et al.2008a, b, c; Latz and Jeong 1996; and referencestherein), and probably confer on them a com-petitive advantage in both coastal and oceanicenvironments.
In the context of the frequently occurring HABspecies (hereafter FOS) recorded in the region;C. furca and C. fusus showed a characteristictransect-specific distribution. C. furca was abun-dant only in the PK transect. C. fusus which waspredominant in the PK transect (Fig. 3b) wasabundant only during October 04 in the CP tran-sect (Fig. 4a).
C. furca and C. fusus are characteristicallyfound in stable stratified water columns (Baeket al. 2006, 2007). However, both species differ inseveral characteristics. In recent observations inSagami Bay, Japan, Baek et al. (2009) reportedthat C. furca had a competitive edge over C.fusus, because of its efficient diel vertical migra-tion capability (a ‘biological’ factor). C. fusus wasstimulated by low salinity and showed dependenceon external environmental conditions such as en-hanced nutrient concentrations following freshwater discharge by heavy rainfall (combination of‘physical’ and ‘chemical’ factors). In light of this,our observations point out that the water mass ofthe PK transect (which is in the northern BOB) isinfluenced by riverine discharge to a much greaterextent compared to the CP transect (in the centralBOB). Additionally, the differential capabilitiesof Ceratium species to acclimatize to such nichescan be an important factor in determining theirdiversity and spatio-temporal distribution.
S. trochoidea, another FOS in the region,was abundant during September/February–March(Fig. 4). September is known as the period ofwithdrawal of SWM, during which cloud coverreduces, whereas March is known for clear skyand with no rainfall. Studies on the factors trigger-ing the growth/bloom formation of S. trochoidea,point to different regulating factors. For e.g., inHong Kong waters, the initiation, maintenanceand disappearance of a S. trochoidea red tide wasnot directly driven by changes in nutrients (Yinet al. 2008). Subsequently, Zhuo-Ping et al. (2009)observed that the cell density of S. trochoideawas positively influenced by high irradiance andfurther enhanced by iron concentration. Theseconditions of high irradiance could possibly beresponsible for the predominance of S. trochoideain March.
Blooms of N. scintillans, yet another FOS inthe region, have been reported from Indian waters(Raghu Prasad 1953, 1956; Santha Joseph 1975;Naqvi et al. 1998; Eashwar et al. 2001; Mohantyet al. 2007; Gomes et al. 2008). Most of theseblooms occurred during the SWM. Sriwoon et al.(2008) observed that N. scintillans blooms in theGulf of Thailand were mainly influenced by theSWM. Since the SWM is a major meteorologi-cal event influencing the BOB, it is absolutely
Environ Monit Assess
necessary to investigate in detail the factors sus-taining the population of N. scintillans in the BOBand their bloom dynamics.
Dinophysis sp., another FOS in the region, wasabundant during March at PK transect (Fig. 4b).Dinophysis are known to increase in cell densityimmediately after a storm-induced mixing event(Nishitani et al. 2005). They can also migratethrough strong gradients and survive under un-favorable conditions (Setala et al. 2005). In a re-cent observation in Portuguese waters, Escaleraet al. (2010) found that the increased numbersof Dinophysis was a result of physically-drivenaccumulation due to long-shore transport. Theyalso found the bloom to be associated with muchwarmer temperatures. In our observation, its pre-dominance during March indicates its preferencefor high temperature since this period is consid-ered a warmer season in the BOB (Narvekar andPrasanna Kumar 2006).
Given that the FOS observed in our studyranged from 0–40 cell L−1, their presence maynot be a population growth issue, as suggestedby Smayda (2002). However, they may play asignificant role in the development of pelagic seedbanks of vegetative cells (Smayda 2002), whichcan serve as inocula for bloom events elsewhere,on the onset of favorable conditions. An earlierstudy (Avaria 1979) suggested that the Chileanfrontal zone located 100 km offshore supporteda P. micans bloom. Transport of offshore-seededProrocentrum and Ceratium blooms to inshorewaters (Pitcher and Boyd 1996) also supports theabove assumption.
Another intriguing aspect to be consideredis the enhancement of phytoplankton biomassto bloom levels by physical processes occurringin the BOB like eddies (Gomes et al. 2000;Prasanna Kumar et al. 2004) and cyclones (Madhuet al. 2002; Vinayachandran and Mathew 2003;Rao et al. 2006). In both eddies and cyclones,bloom formation takes place due to transportof nutrients from bottom layers to the surface.During cyclones, due to strong wind speed, thestratified layer breaks and deepens the mixedlayer, leading to introduction of nutrients intothe surface layers whereas during eddies, Ekmanpumping plays an important role in transport-ing nutrients to surface waters. Eddies are most
likely to occur during the SWM (Prasanna Kumaret al. 2004) whereas cyclones are common duringNovember (Madhu et al. 2002; Vinayachandranand Mathew 2003; Rao et al. 2006). The combi-nation of such physical effects including turbu-lence and advection, with the diverse behavioralcharacteristics of dinoflagellates (e.g., migration,physiological adaptation) holds the key to un-derstanding HAB dynamics in stratified oceanicareas. Even though some of these physicalprocesses may play a crucial role in the formationof HABs, these processes are not well definedand thus knowledge in this context remains weak(GEOHAB 2003). For example, the above stud-ies were based on remote sensing (chlorophyll a)and primary productivity values and none of thereported blooms/enhancement of phytoplanktonbiomass was taxonomically characterized. In thiscontext, the present investigation pointing out thepresence of N. scintillans and C. furca duringNovember (Table 1) further strengthens theirprobable candidature for bloom formation in theregion.
However, it should be noted that the presentfindings are based on the surface water distribu-tion of dinoflagellates from the BOB, but takingin to account the fact that phytoplankton tend togather more in sub-surface rather than surface wa-ters, future studies on the depth-wise distributionof dinoflagellates and notably, HAB species, willbe a step forward.
Conclusions
The present study is the first of its kind detailingthe HAB species from the stratified surface wa-ters of the BOB and their seasonal occurrence.The frequently occurring HAB species indicatetheir ability to survive even under such conditions;their low abundance in the region may not bea growth issue but they may serve as inoculafor blooms if coupled with population triggeringphysical processes like eddies and cyclones in theregion. In this scenario, the characteristic ability ofFOS like C. furca and N. scintillans and their pre-dominance during cyclone-prone months, maketheir candidature stronger for future blooms in theregion.
Environ Monit Assess
Acknowledgements We are grateful to Dr. S.R. Shetye,Director of the National Institute of Oceanography (NIO),for his support and encouragement. We are thankful to ourcolleagues of the department and cruise participants fortheir help at various stages of the work. We acknowledgethe funding support received from the Ministry of EarthSciences (MOES) under the Indian XBT program andthe Ballast water management program, funded by theDirectorate General of Shipping, India. RKN is grateful toCSIR for awarding the senior research fellowship (SRF)and also to POGO-SCOR for providing a fellowship toavail phytoplankton taxonomy training in SZN, Italy. Thisis an NIO contribution (No. 4894).
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