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Bloom-IJMS -2010
Transcript of Bloom-IJMS -2010
Indian Journal of Marine Science
Vol. 39(3), September 2010, pp. 323-333
Bloom of Trichodesmium erythraeum (Ehr.) and its impact on water quality and
plankton community structure in the coastal waters of southeast coast of India
A K Mohanty1, K K Satpathy
1, G Sahu
1, K J Hussain
1, M V R Prasad
1 & S K Sarkar
2
1 Indira Gandhi Centre for Atomic Research, Kalpakkam, Tamil Nadu- 603 102 India 2 Department of Marine Science, University of Calcutta, Kolkata- 700 019 India
[Email: [email protected]]
Received 14 September 2009; revised 11 January 2010
An intense bloom of Trichodesmium erythraeum was observed in the coastal waters (about 600 m away from the shore)
of southeast coast of India during the post-northeast monsoon period. The bloom appeared during a relatively high
temperature condition with coastal water salinity > 31 psu. A significant reduction in nitrate concentration was noticed
during the bloom period, whereas, relatively high concentration of phosphate and total phosphorous was observed. An
abrupt increase in ammonia concentration to the tune of 284.36 µmol l-1 was observed which coincided with the highest
Trichodesmium density (2.88 × 107 cells l-1). Contribution of Trichodesmium to the total phytoplankton density ranged from
7.79% to 97.01%. A distinct variation in phytoplankton species number and phytoplankton diversity indices was noticed.
The lowest diversity indices coincided with the observed highest Trichodesmium density. Concentrations of chlorophyll-a
(maximum 42.15 mg m-3) and phaeophytin (maximum 46.23 mg m-3) increased abnormally during the bloom.
[Key words: bloom, phytoplankton, tropical, Trichodesmium, oligotrophic, cyanobacteria]
Introduction
Trichodesmium erythraeum, a marine
cyanobacterium, is an important nitrogen-fixer in the
sea. It is one of the common bloom-forming species
found in tropical and sub-tropical waters, particularly
in the eastern tropical Pacific and Arabian Sea,
contributing > 30% of algal blooms of the world1.
Estimated global nitrogen fixation by Trichodesmium
bloom (~ 42 Tg N yr-1
) and during non-bloom
conditions (~ 20 Tg N yr-1
) suggests that it is likely to
be the dominant organism in the global ocean
nitrogen budget1, 2
. Trichodesmium normally occurs in
macroscopic bundles or colonies and blooms formed
by it are often extremely patchy. The patchy spatial
distribution of plankton blooms is usually connected
to the physical variability of the water body3.
Reports in literature showed frequent occurrence of
Trichodesmium blooms in Indian waters, however, it
has been reported more frequently in the west
coast4, 5, 6-11
as compared to east coast12, 13-15
. Equipped
with buoyancy regulating gas vesicles and nitrogen
fixation enzymes, Trichodesmium is regarded as an
organism well adapted to stratified, oligotrophic
conditions2. All the available reports on
Trichodesmium bloom from east and west coast of
India have been observed far away from the coast
(> 30 km). This appears to be the second report of
Trichodesmium bloom which was sighted near the
coast similar to the last year report from the same
locality15
.
During a regular coastal water monitoring program,
a prominent discoloration of the surface water was
noticed in the coastal waters of Kalpakkam (12o
33' N
Lat. and 80o
11' E Long) (Figure 1) on 19th February
2008. The bloom was very dense and created
yellowish-green coloured streaks (Figure 2a) of about
4 to 5m width and 10-20m long patches. The entire
bloom extended to several kilometers along the coast.
The phytoplankton responsible for discolouration was
identified as Trichodesmium erythraeum (Figure 2b).
Though, bloom of Noctiluca scintillans16
, Asterionella
glacialis17
and Trichodesmium erythraeum15
in the
coastal waters of the Kalpakkam have been reported,
the present one has many interesting features.
Although, the data collected during our regular work
were not concerned directly with an investigation into
the causes of the bloom, the interest stimulated from
the studies of various physicochemical and biological
characteristics of the coastal water justifies the
purpose of this paper. The acumen in investigating
Trichodesmium bloom appearance and distribution
stems from the recent report about its harmful nature,
INDIAN J. MAR. SCI., VOL. 39, No, 3, SEPTEMBER 2010
324
sometimes causing damages to coastal fish and shellfish
fauna18
. Thus, studying the causes that favour the
appearance of this bloom has social and economical
connotations. The impact of bloom on coastal water
quality and phytoplankton community is reported in this
paper along with the characteristic feature of the bloom.
Fig. 2a & b Discolouration of coastal water of Kalpakkam by Trichodesmium erythraeum bloom patches (a); magnified view of
bundles formed by trichome (b)
Fig. 1 Study area showing the sampling location
MOHANTY et al.: BLOOM OF TRICHODESMIUM ERYTHRAEUM (Ehr..) AND ITS IMPACT ON WATER QUALITY
325
Materials and Methods
Surface water samples were collected twice daily
(between 9 to 10 AM and 4 to 5 PM during the bloom
period (19th to 23
rd February), whereas, during pre-
and post-bloom periods samples were collected
weekly only in the morning hours. Samples were
drawn by lowering a clean plastic bucket from the
Jetty of Madras Atomic Power Station (MAPS) and
analyzed for various physicochemical parameters.
Temperature was measured by a mercury
thermometer with an accuracy of ±0.1oC. Winkler’s
method19
was followed for the estimation of DO.
Salinity was estimated by Knudsen’s method19
. pH
was measured by a pH meter (CyberScan PCD 5500)
with an accuracy of ±0.1. Dissolved nutrients such as,
nitrite, nitrate, ammonia, silicate and phosphate along
with total nitrogen (TN) and total phosphorous (TP)
were estimated following the methods of Grasshoff
et al.19
and Parsons et al.20
. Chlorophyll-a and
phaeophytin were measured spectrophotometrically
(Parsons et al., 1984. The phytoplankton density was
estimated using Utermohl’s sedimentation technique21
and counted using Sedgwick Rafter counting chamber
with the aid of binocular research microscope (Nikon
Eclipse-50i). The identification of phytoplankton
was done by following standard taxonomic
monographs such as Desikachary22
for diatoms;
Subramanian23,24
for dinoflagellates and Fristch
25
for green and blue-green algae (Cyanobacteria).
Three diversity indices such as species richness (R),
species diversity (D) and evenness (J) were computed
to evaluate the variation between phytoplankton
community structure and diversity, using standard
formulae of Gleason (1922), Shannon-Weaver (1963)
and Pielou (1966) respectively.
Results and discussions A. Hydrography
The values of pH did not show significant
variations and ranged from 8.0-8.2 during the study
period (Figure-3a). It did not show any correlation
with bloom appearance as it remained almost stable
during pre-bloom, bloom and post-bloom periods.
The surface water temperature during the study period
ranged from 27.2-32.6°C (Figure 3b). Comparatively
high temperatures were noticed during the afternoon
collections. A general increase in water temperate was
noticed from January to March, which is a general
phenomenon associated with air temperature in this
locality during this period of the year. Most of the
marine cyanobacteria exhibit substantial growth in the
temperature ranges 25-35°C11
. The present bloom was
noticed during relatively high temperature conditions
(28.4-28.7°C in the morning and 31.2-32.6°C in the
afternoon). Temperature has long been recognized as
an important factor that controls Trichodesmium
abundance26-27
. Generally bloom of this filamentous
alga occurred during hot weather season13
,
as
cyanobacteria require relatively high temperature for
its optimum growth compared to other
phytoplankton28-29
. The present study agreed well with
earlier reports4, 13-15, 30
, which showed similar
temperature conditions with the appearance of
Trichodesmium bloom during early summer and
spring31
in the coastal waters of India. As observed,
the bloom was more predominant during afternoon
period when the temperature was relatively high as
compared to morning period.
The observed salinity ranged from 31.58-33.18 psu.
A gradual increase in salinity was noticed during the
study period (Figure 3b). Stable salinity condition
close to typical value of 32 psu and above is known to
Fig. 3a
INDIAN J. MAR. SCI., VOL. 39, No, 3, SEPTEMBER 2010
326
support the growth and abundance of Trichodesmium.
It is well known that the cyanobacterium is a
stenohaline form with optimum growth at > 33 psu
and can’t survive in low salinities11-14
. DO
concentration ranged from 6.2-8.1 mg l-1
(Figure 3a). The lowest and the highest DO
concentration was observed during the post-bloom
and bloom period respectively. Marginally high DO
was noticed during the bloom compared to the pre-
and post-bloom period. However, concentrations of
DO during pre-bloom period were relatively high as
compared to post-bloom period. This could be due to
photosynthetic release of oxygen by the dense algal
biomass. Similar increase of DO content during
Trichodesmium bloom has also been reported
earlier2,15
. As expected relatively low DO contents
were observed during the post-peak bloom period,
indicating that some of the cells are in decayed stage.
This phenomenon of observation of low DO values
near bloom area is common to post-bloom era and
indicative of decayed phase of the bloom.
B. Nutrients Nitrate concentrations ranged from 0.17–6.79
µmol l-1
, the highest value being observed during the
pre-bloom period and the lowest during the bloom
(Figure 3c). Relatively low nitrate levels, continuous
patches with yellowish green colour and increased
primary production (as reflected in chlorophyll-a
values) coinciding with peak bloom period
sufficiently indicated that the bloom was in growth
phase. A significant reduction in nitrate concentration
was noticed during the bloom as compared to pre- and
post-bloom periods. Similar reduction of nitrate
concentration during Trichodesmium bloom has also
been reported by others12,14-15
. Insignificant variation
in concentration of nitrite was noticed during the
period of study. On the contrary, ammonia values
Fig. 3b
Fig. 3c
MOHANTY et al.: BLOOM OF TRICHODESMIUM ERYTHRAEUM (Ehr..) AND ITS IMPACT ON WATER QUALITY
327
were significantly high during the bloom, especially
on the day of the highest cell density, compared to the
pre- and post-bloom observations (Figure 3d), which
ranged from 0.22-284.36 µmol l-1
. This could be
ascribed to the diazotrophic nature of Trichodesmium,
which has the ability to produce ammonium through
the process of nitrogen fixation32
. As a result of the
above process, the observed TN concentration was
also relatively high (392.80 µmol l-1
) on the peak
bloom day (Figure 3d). Surprisingly, perusal of a
plethora of literature available from Indian coasts
revealed that ammonia concentration during
Trichodesmium bloom has rarely been estimated or
reported4, 8, 33
. A comparison of the present ammonia
concentration with that of earlier reported value
(126.72 µmol l-1
) during Trichodesmium bloom from
the same locality15
showed a two fold increase.
Many reports have indicated discolouration of water,
production of offensive smell, increase in ammonia
content and fish mortality in coastal waters due to
Trichodesmium bloom11
. During the present
observation, in spite of prevalence of very high
ammonia content, there was however, no fish
mortality and thus social and economical implications
were minimal. Considering the fact that, ammonia
concentration >0.1 mg l-1
is toxic for the fish
community18
, the bloom could have a significant
adverse effect on the biota of the coastal waters had it
continued for a longer period. No report of fish
mortality or any such nuisance incidence during the
present study could be attributed to factors like
shorter period of bloom persistence and its drifting
away along with the pole-ward water current.
Phosphate levels ranged from 0.09 µmol l-1
during
the pre-bloom to 1.51 µmol l-1
during the bloom
(Figure 3e). The peak coincided with the day of the
Fig. 3d
Fig. 3a-e Variations in physico-chemical properties of the coastal waters of Kalpakkam during appearance of Trichodesmium
erythraeum bloom.
INDIAN J. MAR. SCI., VOL. 39, No, 3, SEPTEMBER 2010
328
highest Trichodesmium cell density. It did not show a
clear trend during the study. Phosphate constitutes the
most important inorganic nutrient that can limit the
phytoplankton production in tropical coastal marine
ecosystems34
and thereby the overall ecological
processes. Usually seawater serves as the main source
of phosphate in estuarine and coastal waters except
those receives fresh water contaminated with
phosphate. Apart from the physical and chemical
processes, phosphate concentration in coastal waters
mainly depends upon phytoplankton uptake and
replenishment by microbial decomposition of organic
matter. In the present study, an abrupt increase in
phosphate content was encountered on the day of
highest cell density compared to other observations.
This increase in phosphate could be due to the
extracellular release35
and decomposition of plankton.
Moreover, bacterial liberation of phosphate from dead
organisms has also been reported to be responsible for
enhanced levels of phosphate during blooms36
. Many
other authors have also reported similar increase of
phosphate content during the occurrence of bloom of
Trichodesmium14-15,35
, Noctiluca37-39
and
Asterionella17
. The irregular trend observed in
phosphate concentration during the study could be
due to its rapid uptake as well as replenishment
processes taking place in the coastal waters. Total
phosphorous concentration showed a trend similar to
that of phosphate and ranged from 0.14-2.83 µmol l-1
(Figure 3e).
Silicate values ranged from 7.58-16.28 µmol l-1
with
lowest and highest values being observed during bloom
and post-bloom periods respectively (Figure 3c). Pre-
bloom concentrations of silicate were marginally high
as compared to that of bloom and post-bloom periods.
Silicate, utilized for the formation of the siliceous
frustules of diatoms, constitutes one of the most
important nutrients regulating the phytoplankton
growth and proliferation and ultimately to its
blooming. Relatively high values of silicate observed
during the pre-bloom period could be ascribed to the
silicate rich freshwater input into the coastal water
during the post-monsoon period. Also, during post-
monsoon period, the environmental conditions were
unfavorable for phytoplankton growth, and thus
silicate uptake was negligible leading to enhanced
level of silicate in the coastal waters. Gradually, with
onset of favourable conditions for phytoplankton
growth, silicate uptake increased leading to decrease
in its concentration in the coastal waters as observed
during the present study. Except for the enhanced
concentration levels of silicate during pre-bloom
period, its concentration remained almost stable
during the bloom and post-bloom period.
Observations similar to this have also been reported
by several authors during the appearance of non-
diatom blooms16,37-38
, where silicate remains
unutilized.
C. Phytoplankton community structure
Trichodesmium is considered as an organism well
used to stratified, oligotrophic environment. Thus, its
abundance should be high in the boundary currents and
decrease towards the coast wherein the availability of
nitrogenous nutrients is more. There has not been any
report of T. erythraeum bloom in the coastal zone right
near the coast (within 600 m from the shore). Results
showed that the bloom constituted both individual
trichomes and colonial forms although the later
dominated to the extent of 80-90%. Generally the
trichome length varied from 300-1200 µm. Unlike the
west coast of India wherein phytoplankton bloom is
generally observed during the beginning of SW
monsoon period (May-September), the present bloom
was observed during the end of NE monsoon period.
The present observation coincided with the transition
period during which the coastal water current was
about to change from southerly to northerly direction.
This is the lull period during which the lowest
magnitude of current is observed at this location.
Blooms have been reported to be conspicuous in calm
conditions. These calm conditions assist the trichomes
to form dense rafts on the surface of the sea as has
been observed during this study.
Phytoplankton community showed a distinct
variation in its qualitative as well as quantitative
aspects during the study. In total 69 species of
phytoplankton were identified which comprised of
62 diatoms, 5 dinoflagellates, one silicoflagellatte and
the cyanobacterium Trichodesmium erythraeum. The
population density of phytoplankters ranged from
1.23 × 105 and 2.94 × 10
7 cells l
-1 (Figure 4) showing
more than two order increase during the peak bloom
period. The lowest cell density was observed during
post-bloom period. Surprisingly, Trichodesmium was
found only during the bloom period from 19.02.08-
23.02.08 and was totally absent during the pre- and
post-bloom observations. Contribution of Tricho-
desmium to the total cell count ranged from 7.79 %
(1.10 × 104 cells l
-1) to 97.01 % (2.88 × 10
7 cells l
-1).
MOHANTY et al.: BLOOM OF TRICHODESMIUM ERYTHRAEUM (Ehr..) AND ITS IMPACT ON WATER QUALITY
329
It is well known that Trichodesmium is more abundant
in subsurface layers (20-30 m) as compared to surface
water36
. Though, the present bloom was observed in
coastal waters with much lower depth
(~ 8 m), in order to examine the presence of
Trichodesmium in the subsurface layers, bottom
samples were collected, and found to be absent. The
observed density of Trichodesmium was found to be
significantly higher than the earlier reported value of
3.38 × 106 cells l
-1 by Ramamurthy et al.
13 and
4.80 × 106 cells l
-1 by Krishnan et al.
11. Scrutiny of
published literature showed that, the present observed
density of Trichodesmium is the highest, reported to
date from Indian waters, and surpassed by a factor of
1.75 times from that of earlier reported highest value
(1.75 × 107 cells l
-1) by Santhanam et al.
14 from
Tuticorin Bay.
Community structure of phytoplankton showed that
the number of species on a single observation varied
between 7 species (on the day of highest cell count)
and 24 during the post-bloom period. As expected
relatively less number of species were found during
the bloom as compared to pre- and post-bloom
periods. Similar results have also been reported40
during Asterionella bloom. Interestingly, number of
species were relatively less during the afternoon
collections on all the occasions as compared to the
morning collections. This again emphasized that
certain phytoplankton such as Trichodesmium
erythraeum, which can tolerate relatively high amount
of irradiance in the surface water during afternoon as
compared to morning period1-3,32
. However, species
not tolerant to irradiance, evading the surface water
leading to low species diversity. Based on the
numerical abundance, 30 species were considered as
important contributing 74.19-99.70% of the
population density (Table 1). Out of these
Asterionella glacialis, Nitzschia longissima,
Thalassionema nitzschioides, Thalassiosira decipiens
and Thalassiothrix longissima were present almost
throughout the study period. Species such as
Biddulphia heteroceros, Cocconeis distans and
Leptocylindrus minimum were found only during the
pre-bloom period and totally absent during bloom and
post-bloom periods. On the contrary, two species of
Biddulphia (B. aurita and B. rhombous) were found
only during the post-bloom period. This clearly
indicated that presence of Trichodesmium erythraeum
favours growth of a selected group of diatoms during
the post-bloom period.
Distinct variations in all the three diversity indices
were noticed during the study period (Figure-5).
Fig. 4 Total phytoplankton density, density of Trichodesmium erythraeum and number of species observed during the bloom
INDIAN J. MAR. SCI., VOL. 39, No, 3, SEPTEMBER 2010
330
Table 1 Percentage contribution of dominant phytoplankton species, total cell density and number of species encountered during the
Trichodesmium erythraeum bloom in the coastal waters of Kalpakkam
14.02.08 19.02.08
M
19.02.08
E
20.02.08
M
20.02.08
E
21.02.08
M
21.02.08
E
22.02.08
M
22.02.08
E
23.02.08
M
28.02.0
8 M
Asterionella
glacialis
21.98 16.48 1.14 3.75 14.40 20.66 5.59 21.52 30.43 24.68 12.90
Biddulphia
aurita
4.84
Biddulphia
heteroceros
1.10
Biddulphia longicuris 0.06 2.42
Biddulphia mobiliensis 2.42
Biddulphia rhombus 1.30 4.03
Chaetoceros
lorenzianus
0.42 2.25 2.42
Chaetoceros sp 0.19 1.13 1.38 1.61
Cocconeis distans 1.10
Coscinidiscus sp 1.10 0.19 2.42
Cyclotella sp 1.30
Dictyocha sp 2.60
Guinardia flaccida 1.61
Leptocylindrus
minimum
0.90
Licmophora gracilis 2.20
Melosira sulcata 2.20 0.33 6.49
Melosira sp 16.81
Nitzschia longissima 3.30 1.48 0.98 3.19 16.00 5.36 1.97 6.33 14.49 2.60 1.61
Nitzschia sigma 2.20 0.60 1.43 2.53
Nitzschia stagnorum 1.10 1.27
Pinnularia interrupta 1.32
Pleurosigma sp 1.27
Pseudonitzschia
delicatissima
0.59 5.07
Pseudonitzschia
pungens
1.13
Thalasiossira
decipiens
12.09 0.26 0.09 0.80 0.25 8.86 8.70 6.49 8.87
Thalasiossira sp 12.09 0.53 0.04 0.19 2.40 1.74 0.66 1.27 4.35 7.79 10.48
Thalassionema
nitzschioides
24.18 4.69 0.34 2.06 16.00 15.05 8.88 17.72 21.74 24.68 13.71
Thalassiothrix
frauenfeldii
4.40 0.45 0.09 1.13 1.06 0.99 1.27 5.19 2.42
Thalassiothrix
longissima
0.41 0.94 2.40 2.04 2.53 1.30 2.42
Trichodesmium
erythraeum
0.00 44.04 97.01 75.80 33.60 43.43 74.67 17.72 13.04 7.79 0.00
% contribution of
above sp.
89.01 88.19 99.70 96.81 85.60 92.47 94.08 82.28 92.75 92.21 74.19
Total cell density
(X 105)
1.29 13.91 294.05 6.89 1.46 8.28 5.63 1.29 1.23 1.37 2.02
Total No. species in
the sample
16 19 7 18 9 16 13 12 8 13 24
M= morning collection, E= evening collection
MOHANTY et al.: BLOOM OF TRICHODESMIUM ERYTHRAEUM (Ehr..) AND ITS IMPACT ON WATER QUALITY
331
Relatively high values of all the indices during the
pre- and post-bloom periods showed that the
phytoplankton community was floristically rich
during these periods. A significant decrease in
diversity indices was noticed on the day of the highest
Trichodesmium density. This could be attributed to
the dominance of Trichodesmium and the presence of
very less number of other phytoplankton species.
E. Photosynthetic pigments Photosynthetic pigments such as chlorophyll-a and
phaeophytin showed wide variations which ranged
from 1.21-42.15 mg m-3
and 0.78-46.23 mg m-3
respectively (Figure 6). The highest concentration was
encountered during the bloom which coincided with
highest cell density. In general, concentration of
chlorophyll-a and phaeopigments remained high
during bloom as compared to pre- and post-bloom
periods and the peak values of these two pigments
were about 20 times higher than the normal values.
Interestingly, concentrations of these pigments were
relatively high during the post-bloom period as
compared to the pre-bloom period. This affirmed the
fact that phytoplankton growth gradually increased
from post-monsoon to summer in this part of Bay of
Bengal10-11
. Similar observations of unusually high
pigment concentrations have been reported by
Ramamurthy et al.13
, Pant & Devassy35
and Satpathy
et al.15
during Trichodesmium bloom and Mishra
et al.40
and Mishra & Panigrahy41
during Asterionella
bloom.
Conclusion Relatively high temperature, low current
magnitude, stable salinity (~ 33 psu) and low nitrate
concentration were observed during the bloom of
Fig. 5 Variations in phytoplankton diversity indices during the bloom period
Fig. 6 Chlorophyll-a and phaeophytin fluctuations during the appearance of bloom
INDIAN J. MAR. SCI., VOL. 39, No, 3, SEPTEMBER 2010
332
cyanobacterium T. erythraeum in the coastal waters of
Kalpakkam. Abnormally high concentration of
ammonia observed during the bloom period was a
concern. The cell density was found to surpass all the
earlier reported densities from east and west coast of
India. Appearance of T. erythraeum in coastal waters
of east coast of India during two successive years
necessitates the need for continuous monitoring of
physico-chemical parameters on a long-term basis,
which would help in comprehending its cause and its
ecological significance.
Acknowledgement
Authors are grateful to Director, Indira Gandhi
Centre for Atomic Research and Director, Safety
Group for their encouragement and support. Help
rendered by Shri. S. Bhaskar of Environmental and
Industrial Safety Section is also duly acknowledged.
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