Download Dynamics of potentially harmful phytoplankton in a semi

Bull Mar Sci. 91(2):141–166. 2015
http://dx.doi.org/10.5343/bms.2014.1041
research paper
Dynamics of potentially harmful phytoplankton
in a semi-enclosed bay in the Sea of Oman
1
College of Agricultural and
Marine Sciences, Sultan Qaboos
University, P.O. Box: 34, Al-Khod
123, Sultanate of Oman.
2
Rosenstiel School of Marine &
Atmospheric Science, University
of Miami, 4600 Rickenbacker
Causeway, Miami, Florida 33149.
Corresponding author email:
<[email protected]>.
*
Date Submitted: 15 May, 2014.
Date Accepted: 9 December, 2014.
Available Online: 26 February, 2015.
Khalid A Al-Hashmi 1 *
Sharon L Smith 2
Michel Claereboudt 1
Sergey A Piontkovski 1
Adnan Al-Azri 1
ABSTRACT.—The dynamics of potentially harmful
phytoplankton in relation to environmental parameters was
investigated in the semi-enclosed Bay of Bandar Khayran (Sea
of Oman) from April 2006 through April 2011. In total, 24
potentially harmful algal species were identified, including
11 species of dinoflagellates and eight species of diatoms. The
dinoflagellates Prorocentrum minimum (Pavillard) Schiller,
1933, Scrippsiella trochoidea Balech ex Loeblich III, 1965,
and Noctiluca scintillans (Macartney) Kofoid and Swezy,
1921 were most abundant during the Southwest Monsoon
(SWM, July–September) and Northeast Monsoon (NEM,
January–March) seasons, while other species occurred in
low abundance and with no clear seasonal patterns. A dense
bloom of Cochlodinium polykrikoides Margalef, 1961 that
affected the distribution and abundance of other harmful
algal species (HAB) was observed for the first time in the Sea of
Oman during 2008–2009. Prorocentrum minimum increased
in abundance during and after the decay of the Cochlodinium
bloom while S. trochoidea was suppressed during this bloom,
increasing thereafter once again. Noctiluca scintillans
disappeared in the late SWM and NEM of 2008 and SWM of
2009, when blooms typically occur annually. Prorocentrum
minimum and S. trochoidea persisted throughout the annual
cycle of all years, enhancing their capability to bloom in the
region under favorable conditions of high light intensities
and relatively warm waters of low turbulence.
Algal blooms are reportedly increasing both in frequency and magnitude in oceanic and coastal waters (GEOHAB 2001, Anderson et al. 2002, Gomes et al. 2009).
Initially, blooms were believed to be restricted mostly to temperate waters, but
since the 1990s a similar trend has been observed in tropical and subtropical regions (Hallegraeff et al. 2004). Coastal ecosystems are becoming more vulnerable
to harmful algal blooms (HABs), especially in enclosed coastal embayments, as a
result of increased nutrient enrichment caused by urbanization, tourism, industrial
wastes, desalination plants, and agricultural activities (Justić et al. 1995, Anderson et
al. 2002, Sellner et al. 2003). Natural processes, such as water circulation, upwelling
Bulletin of Marine Science
© 2015 Rosenstiel School of Marine & Atmospheric Science of
the University of Miami
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relaxation, and cyst formation, are considered important factors contributing to formation of algal blooms (Levinton 2001, Sellner et al. 2003). While some algae are
known to produce toxins that can be accumulated by filter-feeding organisms making them hazardous for humans, blooms of the other (nontoxic) species can result
in high fish mortalities caused by development of low oxygen conditions (Maclean
1993, Claereboudt et al. 2001, Al-Gheilani 2011) or gill clogging and damage due to
mucus secretion and asphyxiation (Maclean 1993, Rensel 1993).
Cell abundances that characterize bloom conditions vary greatly with species
(Smayda 1997). For instance, Dinophysis acuminata (see Table 1 for species authority) and Alexandrium spp. are considered at bloom conditions in Danish waters when
their abundances are 500 cells L−1, but 200 cells L−1 is enough to consider Dinophysis
acuta Ehrenberg, 1839 at bloom condition off Portugal (Anderson 1996). For some
species, low abundance is considered harmful (Hansen et al. 2001). For example, off
the United Kingdom, the mere presence of Prorocentrum lima (Ehrenberg) Dodge,
1975 was sufficient to prompt restrictions on shellfish fisheries (Anderson 1996).
Physical-biological interactions in the coastal ecosystems of Oman are driven
mainly by seasonally reversing monsoon winds (Wiggert et al. 2000). During the
Southwest Monsoon (SWM), southwesterly winds persist during July–September
(Brock and McClain 1992) with average speeds of 10 m s−1 (Krishnamurthi 1981). The
winds then become moderate during October–December in a period known as the
Fall Intermonsoon (FIM), when shallow mixed layers that are depleted in nutrients
occur. During January–March, the Northeast Monsoon (NEM) is characterized by
northeasterly winds, less intense than the SWM winds, but sufficient to cause deep
convective mixing (Banse 1987). Mixing provides nutrients to upper layers making
the productivity of the Arabian Sea relatively high in this season (Burkill et al. 1993).
Later, during April–June, wind speeds are reduced to velocities of approximately 0.25
m s−1, leading to calm seas and a Spring Intermonsoon season (SIM) of low phytoplankton abundance.
In the Arabian Sea (including the Sea of Oman), increased occurrence of coastal
HABs caused by dinoflagellates (e.g., Ceratium spp., Karenia spp., and Noctiluca
scintillans) has taken place since 1976 (Al-Gheilani et al. 2011). Noctiluca scintillans
appears responsible for >50% of HABs, causing fish kills due to oxygen depletion
(Al-Azri et al. 2007, 2012, Al-Gheilani et al. 2011). In Muscat coastal waters, blooms
of N. scintillans are a seasonal event (Al-Azri et al. 2012). Prior to 1997, blooms of
N. scintillans and cyanobacteria (Trichodesmium sp.) reported in the Bay of Bandar
Khayran were accompanied by coral bleaching, development of cancerous growths
on corals (Coles and Seapy 1998), and fish mortalities (Stirn et al. 1996). Cochlodinium
polykrikoides blooms in the Sea of Oman and along the eastern coast of the Arabian
(Persian) Gulf have caused massive fish mortalities, limited traditional fishery operations, impacted coastal tourism, and forced the closure of desalination plants
(Matsuoka et al. 2010, Richlen et al. 2010). In view of these phenomena, it is important to study regional dynamics of HAB species and to investigate relationships
between their abundance and environmental factors. The aim of the present study
was to investigate seasonal and interannual trends in the abundance of potentially
harmful microalgae in the semi-enclosed Bay of Bandar Khayran. The ramifications
of a single and widespread bloom of C. polykrikoides that altered the usual trends of
the frequently appearing HAB species will be discussed.
Al-Hashmi et al.: Dynamics of harmful phytoplankton in the Sea of Oman
143
Figure 1. (A) Map of Oman, (B) coast of Muscat, and (C) the sampling site in the present study.
Methods
The present study was conducted in the Bay of Bandar Khayran (Fig. 1), located
about 25 km from Muscat. Bandar Khayran is a small village at the southeastern
margin of the capital area at 23°30´26˝N and 58°43´48˝E. The bay is mainly a fishing
area with high potential for tourism development. The Bay of Bandar Khayran is the
largest semi-enclosed bay on the western coast of the Sea of Oman with an approximate surface area of 4 km2.
Hydrographic measurements and water samples were carried out at one station
(BK) in the Bay of Bandar Khayran (Fig. 1), at two depths (1 and 10 m), twice a month
from April 2006 through April 2011. Temperature, chlorophyll a, and salinity were
measured with an Idronaut-Ocean Seven 316 CTD probe fitted with an additional
sensor for chlorophyll a fluorescence. Sub-surface water samples representative of
the mixed layer were collected at 1 and 10 m depths with Niskin bottles for analyses of nitrate, nitrite, phosphorus, and silica. Nutrient samples were filtered using
Whatman GF/F filters. Samples were frozen and later analyzed using a five-channel
SKALAR FlowAccess auto-analyzer following procedures described in Strickland
and Parsons (1972) and modified by the manufacturer (Skalar Analytical 1996).
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For phytoplankton species identification and cell counts, water samples (250 ml)
were collected and preserved with 2% Lugol’s iodine solution. Later, samples were allowed to settle and concentrate in 20-mm diameter tubes. Prior to taxonomic analysis, samples were further concentrated using a reverse filtration cone fitted with 1
µm pore-diameter nucleopore filter (Sorokin et al. 1975). Cells were counted in a
Nauman chamber (0.04–0.75 ml) using an inverted Olympus microscope (model
IX50). The cell counts (N ml−1) were determined using the formula: N = (nK), where
n is the abundance of cells of the given species in a sample and K is the coefficient
for the given sample. A coefficient (K) was calculated for each sample: K = (Vs/Vc)/Vf,
where Vs is sample volume, Vc is subsample volume, and Vf is the volume of filtered
water. Identification of harmful species was based on Hallegraeff et al. (2004).
As there was no significant difference in diatom abundance or dinoflagellate abundance between samples collected at the surface (1 m) and at 10 m (paired t-tests
for diatoms: P = 0.93; for dinoflagellates: P = 0.23, respectively), data were averaged
across depths. Samples within each season were also averaged, allowing investigation
of the variability in phytoplankton and environmental parameters in the water column by season. The counts of N. scintillans were not depth averaged because samples
were only collected from the surface. Depth integrated total chlorophyll values (expressed in mg m−2) were calculated from chlorophyll vs depth profiles measured with
a CTD. The Redfield molar ratio was calculated using mean nutrient concentrations.
Principal component analysis (PCA) in Primer 6 (Warwick and Clarke 1991) was
used to correlate phytoplankton community structure with environmental variables
(temperature, salinity, oxygen nitrate, nitrite, silicate, and phosphate). The data were
first log x+1 transformed to reduce the effect of a very abundant species. Data were
normalized by subtracting the mean and dividing by the standard deviation before
the PCA. Correlations were computed using Spearman correlation.
Results
The distribution of temperature in the Bay of Bandar Khayran displayed an annual
cycle with peak temperatures recorded during the SIM and minimum temperatures
during the NEM (Fig. 2A). Warming reached its maximum before the start of the
SWM with the sea surface temperature (SST) increasing to near 30 °C, but above
32 °C in 2007. Due to such intense warming, the surface mixed layer was shallow at
about 8 m. Upwelling during the SWM reduced the SST by about 4 °C from its peak
value during all sampling periods except in 2008 when the SST dropped by 7 °C.
Generally, SST dropped to approximately 23 °C when cool temperatures penetrated
to the bottom during the cooling phase of the NEM. The thermocline was completely
eroded during the winter cooling phase, while during the SWM the thermocline rose
toward the surface indicating an upwelling event (Fig. 2B).
The annual distribution of salinity showed small variations among seasons. The
mean surface salinity fluctuated between 36.5 in January–March (NEM) and July–
September (SWM), and (37.3) in April–June (SIM) and November–December (FIM).
Depth-averaged chlorophyll a had two annual peaks during the NEM and the
SWM periods. The averaged chlorophyll a concentration remained below 1 mg m−3
during the SIM and FIM and approximately 2.5 mg m−3 during most of the NEM and
SWM. In 2010 and 2011, there were exceptionally high concentrations (>4 mg m−3,
Fig. 3). The highest average observed chlorophyll a was 10.5 mg m−3 on 16 December,
Al-Hashmi et al.: Dynamics of harmful phytoplankton in the Sea of Oman
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Figure 2. (A) Monthly mean temperature (°C) in Bandar Khayran Bay (shaded bars correspond
to drop in temperature during the Southwest Monsoon). (B) Annual distribution of temperature
(°C) in Bandar Khyran Bay during 2008, showing intrusion of cold water during the Southwest
Monsoon. Vertical bars denote standard error.
2008, when the highest concentration was 29.13 mg m−3. Highest integrated chlorophyll a over depth during the same period was 156 mg m−2 (Fig. 4).
Averaged nutrient concentrations varied widely seasonally and interannually (Fig.
5). Generally, most nutrients increased in concentration during the SWM and the
NEM seasons, while the SIM recorded the lowest concentrations. Nitrate plus nitrite
(NO3− + NO2−) concentration remained close to 1 μmol L−1 during the SIM season,
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Figure 3. Monthly mean concentrations (and standard errors) of chlorophyll a in from 2006 to
2011 in Bandar Khayran Bay.
while major peaks were observed during the NEM season (4.5–7 μmol L−1). NEM
2010 had the highest recorded NO3− + NO2− concentrations in our study (Fig. 5E).
Concentrations of ammonium (NH4+) fluctuated from 1 to 4 μmol L−1 with higher
concentrations during the FIM. The seasonal distribution of phosphate (PO4−) remained almost stable with concentrations <1 μmol L−1, except during the NEM and
SWM of 2009, when concentrations rose to 1.3 μmol L−1 (Fig. 5 D). Silicate concentrations were mostly 2–3 μmol L−1 except during the NEM 2009 when concentration
Figure 4. Depth integrated chlorophyll a (mg m−2), nutrients concentrations (μM L−1) during the
Cochlodinium polykrikoides bloom. Cells counts (cells L−1) of the bloom are added above each
value of chlorophyll a concentrations. Vertical bars denote standard error.
Al-Hashmi et al.: Dynamics of harmful phytoplankton in the Sea of Oman
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Figure 5. Seasonally averaged concentrations of inorganic nutrients (μM L−1) from 2006 to 2011
in Bandar Khayran Bay. Vertical bars denote standard error.
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was 4.1 μmol L−1 (Fig. 5). Ratios of dissolved inorganic N to inorganic P were usually
less than classical Redfield ratios (16:1) most of the time, except in July and September
2009 and September 2010. Also, the standard ratio of N:Si of 16:16 (Redfield et al.
1963) was >1 during most of the study period except in August and September 2006
when ratios were 0.7 and 1.1, respectively.
Out of a total 287 phytoplankton species encountered in the Bay of Bandar
Khayran, 24 species were identified as potentially harmful, of which 11 were dinoflagellates and eight were diatoms (Table 1). Potentially harmful dinoflagellates
were more abundant than diatoms during the entire sampling period (Figs. 6, 7).
Dinoflagellates increased gradually each year, reaching their highest abundance in
2008 when the C. polykrikoides bloom occurred. After that, harmful dinoflagellates
decreased exponentially (Figs. 6, 8, Table 1).
Large monthly fluctuations were observed in overall dinoflagellate abundances, ranging from 214 to 16 × 103 cells L−1, and up to 400 × 103 cells L−1 during the
December 2008 bloom. Abundance of dinoflagellates also varied seasonally and interannually. Of all four seasons, only the SWM showed consistently higher abundance of harmful dinoflagellates every year (Fig. 8).
Potentially harmful diatoms were rare and found only during FIM of 2006 at different concentrations (Fig. 7, Table 1). Leptocylindrus minimus, Pseudo-nitzschia
delicatissima, and Pseudo-nitzschia pungens all proliferated during a short time period (September 2006), exhibiting abundances of 64 × 103, 51 × 103, and 47 × 103
cells L−1, respectively. Pseudo-nitzschia seriata, Cerataulina pelagica, and Guinardia
delicatula were present at lower concentrations (1500–6500 cells L−1). After 2006,
populations of potentially harmful diatoms decreased significantly (Table 1).
Although 11 potentially harmful dinoflagellates were detected in the Bay, only three
species, Prorocentrum minimum (sensu ITIS.gov), Scrippsiella trochoidea Balech ex
Loeblich III, 1965, and N. scintillans, predominated regularly in the water column.
During our study, massive blooms of C. polykrikoides occurred in the Sea of Oman
in October 2008, but the bloom reached Bandar Khayran Bay only in late November
2008 (late FIM). Because of the sampling schedule, we had only three samples during this C. polykrikoides bloom: November 17, December 2, and December 16, when
the C. polykrikoides counts from the bloom were 20.1 × 104 cells L−1 (max chlorophyll
a = 20.1 mg m−3), 20.6 × 104 cells L−1 (max chlorophyll a = 23.3 mg m−3), and 40.3 ×
104 (max chlorophyll a = 29.17 mg m−3), respectively. These maxima of chlorophyll
a concentration were recorded in the upper water column. The bloom progressively
penetrated to the bottom of the water column with decreased concentration of chlorophyll a (7–15 mg m−3). Four weeks later, the bloom had already decayed and chlorophyll a decreased below 2 mg m−3. However, continuous monitoring of the bloom in
the Muscat area was carried out at several locations (Al-Azri et al. 2014).
The dinoflagellates P. minimum and S. trochoidea were observed throughout
the sampling period with higher abundances during the SWM. This trend of high
abundance was interrupted from December 2008 to January 2009, when the massive blooms of C. polykrikoides occurred. Prorocentrum minimum began increasing
in abundance during the Cochlodinium bloom from 530 cells L−1 in October 2008
(prior to the bloom) to 2800 and 5500 cells L−1 during the bloom in November and
December 2008, respectively. The highest recorded abundance of P. minimum was
8000 cells L−1 in September 2009 (Fig. 9B). The S. trochoidea population was suppressed during the Cochlodinium bloom event, but an increase in abundance of S.
Species
2006
Diatoms
182 (126)
Cerataulina pelagica (Cleve) Hendey, 1927
34 (12)
Chaetoceros coarctatus Lauder, 1864
161 (43)
Chaetoceros curvisetus Cleve, 1889
0
Chaetoceros peruvianus Brightwell, 1856
56 (35)
Cylindrotheca closterium (Ehrenberg) Reimann & J.C.Lewin, 1964
407 (266)
Guinardia delicatula (Cleve) Hasle, 1997
3,514 (2,537)
Leptocylindrus minimus Gran, 1915
1,611 (1,551)
Pseudo-nitzschia delicatissima (Cleve) Heiden, 1928
1,748 (1,715)
Pseudo-nitzschia pungens (Grunow ex Cleve) G. Rittasle, 1993
69 (57)
Pseudo-nitzschia seriata (Cleve) H. Peragallo, 1899
Dinoflagellates
0
Akashiwo sanguinea (K.Hirasaka) G.Hansen & Ø.Moestrup, 2000
6 (5)
Ceratium furca (Ehrenberg) Claparède & Lachmann, 1859
6 (5)
Ceratium fusus (Ehrenberg) Dujardin, 1841
14 (10)
Ceratium tripos (O.F.Müller) Nitzsch, 1817
0
Cochlodinium polykrikoides Margalef, 1961
0
Dinophysis acuminata Claparède & Lachmann, 1859
41 (21)
Dinophysis caudata Saville-Kent, 1881
0
Dinophysis miles Cleve, 1900
25 (16)
Gonyaulax spinifera (Clap. and J. Lachm.) Diesing, 1866
0
Lingulodinium polyedrum (F.Stein) J.D.Dodge, 1989
76 (40)
Noctiluca scintillans (Macartney) Kofoid & Swezy, 1921
13 (11)
Phalacroma rotundatum (Claparéde & Lachmann) Kofoid & Michener, 1911
1,151 (326)
Prorocentrum minimum* (Pavillard) Schiller, 1933
454 (136)
Scrippsiella trochoidea Balech ex Loeblich III, 1965
0
0
0
0
0
194 (138)
0
5 (3)
0
5 (3)
9 (7)
102 (57)
14 (11)
14 (8)
0
0
32 (25)
0
28 (20)
0
1,219 (732)
14 (11)
1,519 (342)
366 (104)
2007
2009
0
5 (2)
0
0
0
0
0
0
13 (5)
0
0
0
0
208 (75)
27 (22)
0
0
0
0
0
36 (21)
23 (13)
173 (80)
65 (44)
62 (28)
23 (19)
4 (3)
5 (3)
56,000 (32,511)
28 (15)
0
5 (3)
18 (14)
28 (25)
9 (7)
14 (8)
18 (14)
14 (7)
9 (7)
19 (12)
141 (87)
90 (47)
0
9 (6)
2,126 (389)
2,394 (588)
383 (133)
1,365 (468)
2008
0
0
9 (7)
5 (3)
9 (8)
0
14 (10)
79 (57)
0
0
5 (4)
46 (22)
19 (12)
0
0
0
9 (6)
0
9 (6)
9 (5)
102 (71)
0
1,324 (298)
389 (127)
2010
Table1. Annual mean abundance (cells L−1) of potentially harmful phytoplankton from 2006–2011 in Bandar Khayran Bay (Standard error in brackets). * sensu
http://www.itis.gov.
Al-Hashmi et al.: Dynamics of harmful phytoplankton in the Sea of Oman
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Figure 6. Monthly averaged abundance (cells L−1) of potentially harmful dinoflagellates from
2006 to 2011 in Bandar Khayran Bay. Vertical bars denote standard error.
trochoidea was observed after the decay of the bloom when cells of S. trochoidea
reached a maximum of 13 × 103 cells L−1 (Fig. 9A).
Noctiluca scintillans formed massive blooms during the SWM and the NEM
throughout the study except in 2008 and early 2009 when C. polykrikoides dominated (Fig. 9C).
Al-Hashmi et al.: Dynamics of harmful phytoplankton in the Sea of Oman
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Figure 7. Monthly averaged abundance (cells L−1) of potentially harmful diatoms from 2006 to
2011 in Bandar Khayran Bay. Vertical bars denote standard error.
Dinophysis caudata, Dinophysis miles, Gonyaulax spinifera, and Neoceratium fusus (Ehrenberg) F.Gomez, D.Moreira & P.Lopez-Garcia, 2010 were rare and present
only in a few months of the year and in low numbers. Dinophysis caudata and G.
spinifera were found only during the SWM of 2006 and 2007. Neoceratium fusus was
rarely found in 2007, 2009, and 2010, and was more abundant during the late SWM
and early NEM of 2008.
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Figure 8. Seasonal concentrations (cells L−1) of potentially harmful dinoflagellates from 2006 to
2011 in Bandar Khayran Bay. Vertical bars denote standard error.
Principal component analysis indicated a clear link (correlation) between increases in P. minimum abundance, nitrate + nitrite increase, and colder temperatures (Fig.
10A). Noctiluca scintillans abundance was also associated with nitrate + nitrite, ammonium, and lower salinity water (Fig. 10B). However, S. trochoidea was less associated with nitrogen and cooler water than other species (Fig. 10C).
Discussion
Identification and enumeration of harmful phytoplankton species, if provided in
the early stage of HAB development, can be used as a tool by government officials
to recommend measures for minimizing the impact of HABs. Early warning allows
managers of coastal establishments such as aquaculture farms and desalination
plants to start their action plans prior to the event. Harmful algal species are distributed among all major taxonomic groups. There are about 50 dinoflagellate species
considered to be harmful (Hallegraeff et al. 2004) and they can produce monospecific, or close to monospecific, blooms that can occur below or at the water’s surface
(Horner 2002).
Most potentially harmful species encountered in the Bay of Bandar Khayran (especially diatom species) were rare. The abundances of the potentially harmful diatoms
L. minimus, P. delicatissima, and P. pungens were restricted to August–September
2006 (SWM season) when N:Si ratios were close to the optimum growth value of 1.0.
N:Si ratios <1 usually result in N limitation and ratios >1 result in Si limitation in the
growth of diatoms (Dortch and Whitledge 1992). Diatoms, in general, have faster
growth rates than the other phytoplankton groups when concentrations of nutrients
and light conditions are optimal (Brand and Guillard 1981). Even though there was a
good supply of nitrogen in the water column, harmful diatom species did not occur
in high abundance (Fig. 7), probably due to a shortage in supply of silicate as N:Si
ratio exceeded three.
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Figure 9. Monthly averaged abundance (cells L−1) of (A) Scrippsiella trochoidea, (B) Prorocentrum
minimum, and (C) Noctiluca scintillans (square-root transformed) from 2006 to 2011 in Bandar
Khayran Bay. Shading corresponds to duration of Cochlodinium polykrikoides bloom in the Bay.
Vertical bars denote standard error.
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Figure 10. analysis showing the associations of inorganic nutrients and other environmental factors with the three major phytoplankton species: (A) Prorocentrum minimum (PC1 34.7%, PC2
24.7); (B) Noctiluca scintillans (PC1 34.8%, PC2 22.1%); and (C) Scrippsiella trochoidea (PC1
30.6, PC2 19.3).
Harmful dinoflagellates were more abundant and dominated the phytoplankton
HAB assemblages in Bandar Khayran Bay most of the time (Figs. 6, 7). This dominance of dinoflagellates over diatoms, all species combined, is a characteristic of
Bandar Khayran Bay (Al-Hashmi et al. 2012) and of Muscat coastal waters (Al-Azri
et al. 2010). Dinoflagellates tend to dominate phytoplankton communities under
low nutrient concentrations (Lalli and Parsons 1997) and high temperatures (Boney
1989). In addition, about half of the species of dinoflagellates are exclusively heterotrophic and feed on bacteria, flagellates, diatoms, and other dinoflagellates (Hansen
1991).
On the interannual scale, it is believed that the contribution of dinoflagellates to
algal blooms is increasing in the Arabian Sea basin, when compared to diatom contributions (Subba-Rao and Al-Yamani 1998, Gomes et al. 2009, Piontkovski et al.
2011). This decline in diatom biomass is the result of a decline in the availability of
Al-Hashmi et al.: Dynamics of harmful phytoplankton in the Sea of Oman
155
nitrate caused by increased thermohaline stratification assocaiated with rising temperatures (Smayda 1997). Most of the HAB events in Oman’s coastal waters have
been dominated by dinoflagellates, with N. scintillans occurring most commonly
(Al-Gheilani et al. 2011, Al-Azri et al. 2012). This species frequently occurred in
blooms in the Arabian Sea as well (Gomes et al. 2009).
Bloom of Cochlodinium polykrikoides.—A devastating bloom of C.
polykrikoides appeared for the first time in the Sea of Oman in August 2008, lasted
until August 2009, and expanded into the Arabian Gulf and along the Iranian coast
(Matsuoka et al. 2010, Richlen et al. 2010, Fatemi et al. 2012, Hamzei et al. 2012) and
into the Arabian Sea at least as far as Masirah Island. The bloom reached Muscat
coastal waters in November 2008 (Al-Azri et al. 2014). Ballast water has been suggested as a possible mechanism for introducing this species to the region (Richlen et
al. 2010). The bloom resulted in massive fish mortalities and huge economic losses
(closed desalination plants, electric power stations, and tourist sites). The bloom
reached the Bay of Bandar Khayran in late November 2008 and dissipated by the end
of January 2009. The appearance of the bloom was indicated by the increase of chlorophyll a from 2.8 to 20.5 mg m−3. The maximum concentration in the bay was 29.12
mg m−3, which is four times lower than the maximum concentration recorded in
some sites around Muscat during the bloom event (Al-Azri et al. 2014). The sampling
regime of the present study (twice per month) likely hindered us from recording the
peak of the bloom inside the bay. Also, the C. polykrikoides bloom likely was advected
to the bay in lower concentrations than offshore because of the narrow opening of
the bay and its semi-closed circulation.
It has been suggested that intense upwelling off Oman in the SWM was an important factor contributing to the initiation and proliferation of this C. polykrikoides
bloom, and that the bloom was pushed toward the coastal areas by anticyclonic eddies (Al-Azri et al. 2014). In Omani coastal waters, the bloom reached its highest
concentrations during the FIM and sustained its growth during most of the NEM
period. It was first reported from Iranian coastal waters in October 2008 in a temperature range of from 21.8 to 28.9 °C (Fatemi et al. 2012). However, the bloom in
the offshore waters of the Muscat coast occurred in unusually warm water, >30 °C,
during the first week of observation of the bloom and at salinity values ranging from
36.82 to 37.39 (Al-Azri et al. 2014). In Bandar Khayran Bay, the temperature and
salinity during the bloom were 23.6 to 26.65 °C and 36.6 to 36.9, respectively. This
variation in temperatures between the offshore waters and the bay occurred because:
(1) the bloom reached the bay a month later than its occurrence in the offshore area;
and (2) it appeared in the Bay at the start of the NEM when convection often causes
cooling.
Although investigation has shown that blooms of C. polykrikoides in the Chesapeake
Bay have coincided with rainfall, low wind conditions and associated stratification
(Mulholland et al. 2009), the C. polykrikoides bloom in Bandar Khayran Bay, and the
Sea of Oman in general, occurred at substantially higher salinity (36.6–37.39), but
within a similar temperature range. Of the other areas of the globe experiencing C.
polykrikoides blooms, only the western Pacific Ocean has temperature and salinity
conditions similar to Oman (Table 2). The bloom in the central Sea of Oman occurred during the relatively quiescent FIM, but by the time it was advected into the
bay, the more windy conditions of the NEM prevailed. These reports confirm the
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ability of C. polykrikoides to tolerate very wide ranges of temperature and salinity
(Kim et al. 2004, Kudela et al. 2008).
The Chesapeake Bay events also coincided with elevated nutrient conditions.
Similarly, all nutrients in Bandar Khayran Bay were elevated during the arrival of the
bloom and then decreased during the bloom. NO3− + NO2− concentrations were high
during the early weeks of the bloom, but decreased during the following weeks when
most of nutrients had been utilized.
The nutrient concentrations in the bay during the bloom were less than half the
concentrations at the initiation of the bloom in coastal waters offshore of Muscat (AlAzri et al. 2014) and four-times lower than the values reported from Iranian coastal
waters (Fatemi et al. 2012). The mixotrophic ability of this species may have contributed to its rapid and sustained growth during the period of low nutrient concentrations as mixotrophy has been shown to double the growth rate of C. polykrikoides
(Jeong et al. 2004). The phosphate concentrations in Muscat coastal waters is stable
ranging from 0.5–1.5 μM L−1 (Al-Azri et al. 2010, Al-Hashmi et al. 2012). No pronounced elevation of phosphate was recorded during the bloom in the Bay; however,
an elevated phosphate concentration of 3–7 μM L−1 was recorded off Muscat during
the initiation of the bloom (Al-Azri et al. 2014). Elevated concentrations of phosphate
(more than five times the typical concentration) during this Cochlodinium bloom
also reported from Iranian waters (Fatemi et al. 2012) indicating a general association of C. polykrikoides with elevated phosphate concentration (Gárate-Lizárraga et
al. 2004).
Aside from economic losses, no comprehensive study investigated the effect of
the C. polykrikoides bloom on the marine organisms in Bandar Khayran Bay. Even
though shifts in the occurrence of coral species was noticed, soft corals replaced
hard corals in some parts of the Bay (M Claereboudt, Sultan Qaboos University, unpubl data), there is no clear evidence linking this coral species’ shift directly to the
C. polykrikoides bloom event. The bloom, however, affected the distribution of other
HAB species in the Bandar Khayran Bay. Here we discuss the most frequently occurring HAB species (S. trochoidea, P. minimum, and N. scintillans) in more detail.
Scrippsiella trochoidea.—Scrippsiella trochoidea was reported frequently, but
in low abundance (<100 cells L−1), although this species can reach concentrations of
300–700 cells L−1 during the SWM period in Bandar Khayran Bay (Al-Hashmi et
al. 2012). In the present study, S. trochoidea had a mean monthly occurrence of 600
cells L−1 and reached a peak of 1000–2000 cells L−1 during the SWM, responding to
the marginal increase in nutrient concentrations. Scrippsiella trochoidea was also a
dominant component of the phytoplankton during the early SWM in the southern
Sea of Oman (Stirn et al. 1993). The abundance of this species remained stable during
most of our sampling period, but decreased in abundance during the C. polykrikoides
bloom period (December 2008–January 2009) (Fig. 9A). This was presumably due
to the allelopathic properties of the C. polykrikoides bloom. Allelopathic effects of
C. polykrikoides blooms on phytoplankton species, including S. trochoidea, include
loss of motility, distortion of cell morphology, and cell mortality (Gobler et al. 2008,
Tang and Gobler 2010). On the other hand, high abundance of S. trochoidea was recorded in early May 2009 (8 × 103 cells L−1) after an unusual increase in nutrients during the SIM season. This increase in nutrient concentrations during the SIM period,
known for low nutrient conditions, was the result of the decay of the C. polykrikoides
Al-Hashmi et al.: Dynamics of harmful phytoplankton in the Sea of Oman
157
Table 2. Different ranges of temperature (°C) and salinity during Cochlodinium polykrikoides
blooms in various locations.
Location
Temperature
Western Pacific
18.0–30 .0
Peconic Estuary and Shinnecock Estuary 20.0–25.0
Chesapeake Bay
27.0–29.5
Sea of Oman (Iran coast)
21.8–28.9
Sea of Oman (Oman coast)
22.6–30.7
Salinity
30.0–35.8
22.0–30.0
18.9–27.9
37.9–39.0
36.8–37.4
Source
Kudela et al. 2008
Gobler et al. 2008
Mulholland et al. 2009
Fatemi et al. 2012
Al-Azri et al. 2013
blooms. An increase in abundance of some microalgae during bloom degradation
has been documented and is thought to occur because of rapid physiological adaptation in utilization of available nutrients and exudates produced during growth and
decomposition of a bloom (Levinton 2001).
Scrippsiella trochoidea is a cosmopolitan, bloom-forming species widely distributed in coastal waters (Wall et al. 1970, Wang et al. 2008, Gárate-Lizárraga et al. 2009,
Spatharis et al. 2009, Zhuo-Ping et al. 2009). Wide distribution is due to the capability of this species to tolerate a broad range of environmental conditions (Steidinger
and Tangen 1997, Granéli and Turner 2006). For example, temperature and salinity
ranges of 2–30 °C and 5–55, respectively, can be tolerated (Kim and Han 2000, Wang
et al. 2007). Also, this species forms cysts (Matsuoka and Fukuyo 2000) that not
only insure survival of vegetative cells under adverse environmental conditions, but
also provide better opportunities for species’ dispersal and bloom development (Dale
1983, Anderson and Keafer 1985). Even though S. trochoidea is considered “harmless” (non-toxic), it could be harmful in sheltered bays where blooms can cause fish
kills and mass invertebrate mortalities by depleting oxygen levels (Hallegraeff et al.
2004). Blooms of S. trochoidea have often caused massive fish mortality and economic losses worldwide (Spatharis et al. 2009).
Prorocentrum minimum.—Prorocentrum minimum has increased its global
distribution causing massive blooms worldwide (Heil et al. 2005). In the Arabian
(Persian) Gulf, P. minimum is considered a potential bloom-forming or harmful algal
species in Kuwaiti waters (Subba-Rao and Al-Yamani 1998). As for Omani waters, P.
minimum was only once previously reported in the Gulf of Masirah (Arabian Sea)
together with other toxic dinoflagellates that were implicated in fish mortalities in
1992 (Stirn et al. 1993). Here we report a continuous occurrence of P. minimum for
the first time, though studies of phytoplankton in the Muscat region started in 1995.
Presumably, this species was missed during earlier studies due to its small size (14–
22 μm). Commonly, it is difficult to identify the exact time of introduction of a new
harmful species into a region due to the lack of long-term data as well as the possibility of overlooking these species within a particular region when they are new and in
low abundance (Heil et al. 2005).
Prorocentrum minimum was observed throughout the sampling period (2006–
2011) with a periodic increase of abundance in the late NEM and late SWM (Fig.
9B), showing strong association with nitrate increases during these times (Fig. 10C).
Prorocentrum minimum is capable of a wide range of growth rates, but the highest
rates were obtained either under high light conditions or warm temperatures (Heil
et al. 2005). This suggests that P. minimum is a better competitor over other species
due to the relatively warm and calm conditions of Bandar Khayran Bay. Moreover, P.
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minimum has high tolerance for elevated pH (Hansen 2002) and can acquire energy
by mixotrophic feeding (Jeong et al. 2010). Mixotrophy has been recognized as an
important mode of nutrition to supplement nutrients in nutrient poor environments
(Stoecker et al. 2006). Thus, mixotrophy likely enchances the capability of this species to out-compete other strict phototrophs and heterotrophs under limited nutrient conditions (Raven 1997).
Unlike S. trochoidea and N. scintillans, P. minimum was not greatly affected by the
C. polykrikoides bloom. Instead, an increase in the population occurred during the
bloom and its maximum abundance was reached after the decay of the C. polykrikoides bloom (Fig. 9B). Some reports suggest that species such as P. minimum might
co-dominate phytoplankton communities during a C. polykrikoides bloom and immediately after the disappearance of C. polykrikoides blooms (Gobler et al. 2007).
After the decay of a bloom, the community becomes more heterotrophic, as organic
nutrients are released into the water (Riemann et al. 2000). Prorocentrum minimum,
the most persistent mixotrophic species in the bay, is favored in terms of growth
and reproduction by any supply of organic nutrients released by decaying blooms
(Carlsson et al. 1998, Glibert et al. 2001, Heil et al. 2005). Due to its small surface to
volume ratio, P. minimum has another advantage: its ability to take up nutrients even
at very low concentration (Levinton 2001). After October 2009, the abundances of
P. minimum and S. trochoidea were reduced to normal levels, probably due to a decrease in nutrient supply and recovery of grazers, which were earlier reduced because
C. polykrikoides causes strong mortality in zooplankton as well (Jiang et al. 2009).
Noctiluca scintillans.—Blooms of Noctiluca scintillans are common yearly
events in the Sea of Oman (Al-Azri et al. 2007, Al-Hashmi et al. 2010), as well as in
the Arabian Sea (Gomes et al. 2009). Unlike the red N. scintillans, reported from
temperate coastal waters (Harrison et al. 2011), in the Arabian Sea, N. scintillans
appears green because of the photosynthetic symbiont Pedinomonas noctilucae
(Subrahmanyan) Sweeney, 1976 that lives in their vacuoles (Sweeney 1976, Elbrachter
et al.1989, Hausmann et al. 2003). Since Bandar Khayran Bay is connected to the
Sea of Oman through several channels, the Bay is directly affected by blooms of N.
scintillans varying in density and distribution depending on prevailing physical conditions (Al-Azri et al. 2007). Blooms develop twice per year—late SWM (September–
October) and NEM (January–February)—and cell concentrations are generally
higher during the NEM than the SWM, with some interannual variation. In particular, these variations were pronounced and this situation reversed in 2007 when the
density of the bloom was highest during the SWM season (Fig. 9C). Tropical Cyclone
Gonu severely affected the Sea of Oman in June 2007 when it struck the Muscat area.
Increased rainfall, wind velocity, and advection of water masses could enhance the
accumulation of N. scintillans leading to bloom formation (Smayda 1997, Dela-Cruz
et al. 2002, Miyaguchi et al. 2006, Al-Azri et al. 2007). Variation in the abundance of
N. scintillans has been reported from different parts of the world, revealing temporal
variability extending from seasons to years depending on hydrographical conditions
(Uhlig and Sahling 1990, Huang and Qi 1997, Pithakpol et al. 2000).
Blooms of N. scintillans have been reported to correlate with temperature and salinity (Elbrachter and Qi 1998, Miyaguchi et al. 2006). The blooms of N. scintillans in
the present study occurred when water temperatures ranged between 21 and 28 °C.
However, the optimum temperature ranges vary regionally for this species (Huang
Al-Hashmi et al.: Dynamics of harmful phytoplankton in the Sea of Oman
159
and Qi 1997). The salinity range leading to optimal growth of N. scintillans was reported as 29–36. (Miyaguchi et al. 2006). Although salinity levels during all seasons
in the bay were above this optimal range, variations were small and the PCA revealed
a negative correlation between salinity and the abundance of N. scintillans (Fig. 10B).
As with temperature, the optimum salinity concentrations for N. scintillans growth
were reported to be broad and greatly varied among regions (Huang and Qi 1997,
Tada et al. 2004). This variation in the optimum required salinity and temperature
for Noctiluca growth highlights the euryhaline and eurythermal nature of this species (Elbrachter and Qi 1998).
Noctiluca scintillans is a phagotrophic organism; therefore, availability of prey is
also considered a key factor in the abundance variation of N. scintillans (Elbrachter
and Qi 1998). Noctiluca scintillans feeds on phytoplankton, protozoans, copepods,
and copepod eggs (Steidinger and Tangen 1997, Nakamura 1998, Quevedo et al.
1999, Strom 2001). Our analysis revealed a positive correlation between N. scintillans
abundances and nitrogen concentrations in the bay. Noctiluca scintillans blooms occur in nutrient-enriched water either when feeding by phagotrophy during plankton
succession or through carbon fixation by its autotrophic prasinophyte endosymbionts (Gomes et al. 2014). Nitrate levels were reported to be higher in a N. scintillans
bloom in the northeastern Arabian Sea than in a nearby no-bloom area (Matondkar
et al. 2012). The strong correlation with ammonium in the present study may be
related to the high Noctiluca cellular contents of ammonium that Noctiluca uses to
regulate its buoyancy (Montani et al. 1998).
Noctiluca scintillans disappeared from Bandar Khayran Bay after April 2008 and
only re-appeared in low abundance in May 2009, when the usual late SWM-NEM
blooms did not develop. This 1-yr absence coincided with the C. polykrikoides bloom.
It has been speculated that Noctiluca scintillans blooms are initiated at depth in the
proximity of hypoxic waters off the coast of Oman and in the Sea of Oman (Gomes
et al. 2014). They may be brought up to the surface by means of the cold cyclonic
eddy activity of early November–December (Gomes et al. 2008). Once in the surface water, the blooms may eventually be transported to the southern Sea of Oman,
including off the coast of Muscat by anti-clockwise eddies and north-easterly winds
(Gomes et al. 2008).
In November 2008, the Cochlodinium bloom was already well established in the
coastal waters of Oman and before the typical onset of the Noctiluca bloom. Water
temperatures were around 23 °C and dissolved oxygen values were 2.5–3.0 ml L−1.
These unusual conditions were probably more favorable to Cochlodinium than
Noctiluca which typically is known to bloom in waters between 26 and 27 °C and
4–5 ml L−1 of dissolved oxygen. Moreover, the N. scintillans bloom was perhaps not
initiated due to competition and allelopathic effects of C. polykrikoides. Because a
rich food supply is necessary for Noctiluca scintillans to multiply massively (Huang
and Qi 1997), this supply might be suppressed by the same mechanisms. However,
N. scintillans blooms in a bay off Mazatlan, Mexico, co-existed with a harmful dinoflagellate bloom of Gymnodinium catenatum Graham, 1943, although they had
occurred separately earlier (Rodríguez et al. 2005). In Mazatlan Bay, N. scintillans
was actively grazing and rapidly engulfing chains of G. catenatum, causing a decline
in the G. catenatum population.
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Summary.—Twenty-four species of phytoplankton were identified as toxic or potentially harmful in high concentration. Dinoflagellates were the major HAB component of the Bandar Khayran Bay phytoplankton community, while HAB diatom
species, especially L. minimus, P. delicatissima, and P. pungens, were restricted
to 2006. Among dinoflagellates, only three species were found in high concentration during most of the study period: S. trochoidea; P. minimum; and N. scintillans. Noctiluca scintillans is the most common bloom-forming species in the Sea of
Oman, with blooms occurring during the late SWM and the NEM. These seasons
provide the proper environmental factors for the bloom, such as moderate rainfall,
wind, and water mass advection. However, this synchronization was disturbed by the
event of the offshore C. polykrikoides bloom in 2008 causing the N. scintillans bloom
to disappear from the Sea of Oman and hence from the bay. Information on bloom
initiation could be a useful early warning tool, particularly to desalination plants and
the aquaculture industry, to take precautions prior to a bloom’s arrival.
The other HAB species, S. trochoidea and P. minimum, were present during the
seasons with increased abundance during the SWM and NEM when nitrate concentration increased. However, this seasonality was not clearly defined as increase in
abundance was also seen in other seasons, suggesting other factors could affect their
distribution. Our PCA suggested nitrogen the most important environmental factor for blooms of these taxa. Despite the C. polykrikoides bloom event, P. minimum
persisted during the event and both species recovered quickly after the decay of the
Cochlodinium bloom. The permanent residence of these species should be taken into
account when considering the bay status and management. Even though cell concentrations were not at blooming levels and cannot be considered as a threat, there is
always the possibility of increasing eutrophication from future tourism and domestic
waste, which could increase the proliferation of these species.
The introduction of C. polykrikoides to Bandar Khayran Bay was likely a result of
offshore transport and the bloom in the bay might have established a seed bed that
will permit a C. polykrikoides bloom to reoccur under favorable conditions, such
as wind stress during the SWM and NEM. Therefore, it is of great importance to
continue monitoring the distribution and abundance of potential HAB species to
facilitate a comprehensive understanding and to forecast harmful events in coastal
ecosystems. Also, it is important to study the dinoflagellates in the Bay of Bandar
Khayran and Muscat coastal waters to better understand the blooming mechanisms
of these harmful phytoplankton species.
Acknowledgments
We acknowledge the support of the Department of Marine Science and Fisheries, Sultan
Qaboos University for the work reported here. We extend our appreciation to G Hallegraeff,
H Gomes, and J Goes for their review and constructive comments. Thanks to H Al-Habsi
and F Al-Abdli for running the nutrient analyses and the crew of the Research Vessel Al
Jamiah. This research is supported by the grants under the project RC/AGR/FISH/12/01 and
US National Science Foundation grant numbers OCE 0825598 and OCE 1259255.
Al-Hashmi et al.: Dynamics of harmful phytoplankton in the Sea of Oman
161
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