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Abundance of harmful algal blooms in the coastal waters of Oman: 2006–2011

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Abundance of harmful algal blooms in the coastal

waters of Oman: 2006–2011

Adnan R. Al-Azri, Khalid A. Al-Hashmi, Harub Al-Habsi, Nasser Al-Azri & Salim
Al-Khusaibi

To cite this article: Adnan R. Al-Azri, Khalid A. Al-Hashmi, Harub Al-Habsi, Nasser Al-Azri &
Salim Al-Khusaibi (2015) Abundance of harmful algal blooms in the coastal waters of Oman:
2006–2011, Aquatic Ecosystem Health & Management, 18:3, 269-281

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 Abundance of harmful algal blooms in the coastal waters
of Oman: 2006–2011
Adnan R. Al-Azri,* Khalid A. Al-Hashmi, Harub Al-Habsi,
Nasser Al-Azri, and Salim Al-Khusaibi
College of Agricultural and Marine Sciences, Sultan Qaboos University, P.O. Box 34, Al-Khod 123,
Sultanate of Oman
*Corresponding author: [email protected]; [email protected]
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Over the last decade, the ecosystem of the Sea of Oman and Arabian Sea has been showing signs of
rapid and profound changes in terms of phytoplankton diversity and harmful algal bloom outbreaks.
Frequent blooms have been on the rise in the coastal waters of Oman causing adverse impacts on
marine life. The population dynamics of potentially harmful phytoplankton in relation to environmental
parameters was investigated from June 2006 to April 2011. Our studies recorded 24 potentially harmful
species. Dinoflagellates Prorocentrum minimum, Scrippsiella trochoidea, Cochlodinium polykrikoides
and Noctiluca scintillans were the most abundant species. Diatoms Pseudo-nitzschia seriata,
Climacodium frauenfeldianum and Guinardia flaccida were the most abundant, but occurred at low
concentrations. Scrippsiella trochoidea and Noctiluca scintillans were reported previously as common
phytoplankton in Oman coastal waters; however, Prorocentrum minimum and Cochlodinium
polykrikoides are reported for the first time. Here we report their occurrence and persistence in relation
to changes in environmental parameters. In addition, the potential long-term implications of changes in
phytoplankton species and harmful algal blooms outbreaks on ecological, economic, social and human
health impacts will be discussed.

Keywords: Cochlodinium polykrikoides, Prorocentrum minimum, Scrippsiella trochoidea, Noctiluca

scintillans, monsoon, marine life

Introduction et al., 2003). In addition, natural processes such as

water circulation, upwelling relaxation and cyst
Coastal ecosystems are becoming more vulner- formation are also considered important factors
able to harmful algal blooms (HABs), especially contributing to formation of algal blooms (Levin-
in enclosed coastal embayments, as a result of ton, 2001; Sellner et al., 2003). The introduction
increased nutrient enrichment caused by urbaniza- of non-indigenous marine phytoplankton species
tion, tourism, industrial wastes, desalination has been demonstrated to have considerable eco-
plants, agricultural activities and ballast water logical and economic impacts especially in the
(Justic et al., 1995; Anderson et al., 2002; Sellner coastal waters (Halleagraff, 1998; Richlen et al.,

Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/uaem.

269
Aquatic Ecosystem Health & Management, 18(3):269–281, 2015. Copyright Ó 2015 AEHMS. ISSN: 1463-4988 print / 1539-4077 online
DOI: 10.1080/14634988.2015.1027131
 270 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281

2010; Matsuoka et al., 2000). Unlike other marine eastern coast of the Arabian (Persian) Gulf have
invasive species, investigating the introduction of caused massive fish mortalities, limited traditional
non-indigenous phytoplankton species and their fishery operations, impacted coastal tourism, and
impact in marine ecosystem poses substantial chal- forced the closure of desalination plants (Richlen
lenges. While some algae are known to produce et al., 2010; Matsuoka et al., 2000). In view of
toxins which can be accumulated by filter-feeding these phenomena, it is important to monitor
organisms making them hazardous for humans, regional dynamics of HAB species and to investi-
blooms of the other (nontoxic) species can result gate relationships between their occurrence and
in high fish mortalities caused by development of change in environmental conditions
low oxygen conditions (MacLean, 1993; Claere- The aim of this study was to investigate sea-
boudt et al., 2001) or gill clogging and damage sonal and interannual trends in the abundance of
due to mucus secretion and asphyxiation potentially harmful microalgae in the semi-
(MacLean, 1993; Rensel, 1993). enclosed Bay of Bandar Khayran in relation to
In the past several decades, massive expansion environmental conditions and possible role of
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of both diatoms and dinoflagellate blooms has invasive species.

occurred in the Sea of Oman and Arabian Sea
(Thangaraja et al., 2000; Parab et al., 2006; Al-
Azri et al., 2007; Gomes et al., 2008). These Methods
blooms were not observed during the Joint Global
Ocean Flux Study (JGOFS) cruises of the 1990s, Despite the ephemeral nature of HABs and the
but have expanded considerably except for dia- large area to sample (3165 km of coastline, the
toms blooms which showed a decline in a number Sea of Oman and the Arabian Sea), we have
of outbreaks. In general, diatoms blooms are domi- attempted to capture general trends in HABs by
nated by Pseudo-nitzschia seriata, Climacodium sampling bimonthly and during major bloom out-
frauenfeldianum and Guinardia flaccida species, breaks. The bimonthly sampling was carried out at
although their occurrences were in low concentra- one station (BK) in the Bay of Bandar Khayran
tions (Al-Hashmi et al., 2012). Unlike diatoms, (Figure 1), at two depths (1 m and 10 m), from
dinoflagellate blooms have taken place in coastal June 2006 to April 2011. Temperature, chlorophyll
areas since 1976, dominated by Ceratium furca, a and depth were measured with an Idronaut-
Karenia brevis and Noctiluca scintillans (Al-Ghei- Ocean Seven 316 CTD probe fitted with an addi-
lani et al., 2011). In 2000, Ceratium furca, Cera- tional sensor for chlorophyll a fluorescence. An
tium fusus and Karenia brevis have been reported initial CTD cast was performed, before taking
to cause environmental impact and mass mortality water samples, to determine the depth profile and
of marine organisms in the coastal water of Oman identify the mixed layer and thermocline position.
(Thangaraja et al., 2000). Noctiluca scintillans Then, sub-surface water samples representative of
appears responsible for more than 50% of HABs the mixed layer were collected at 2 m and 10 m
causing fish kills induced by oxygen depletion depths with Niskin bottles for analyses of nitrate,
(Al-Azri et al., 2007; Al-Gheilani et al., 2011; Al- nitrite, phosphorus and silica. Nutrient samples
Azri et al., 2012). In Muscat coastal waters, were filtered using Whatman GF/F filters. Samples
blooms of N. scintillans are a seasonal event were frozen and later analyzed using a 5-channel
developing in early spring (Al-Azri et al., 2012). SKALAR FlowAccess auto-analyzer according to
Prior to 1997, blooms of N. scintillans and cyano- procedures described in Strickland and Parsons
bacteria (Trichodesmium sp.) reported in the Bay (1972) and modified by the manufacturer (Skalar
of Bandar Khayran were accompanied by coral Analytical, 1996).
bleaching, development of cancerous growths in For phytoplankton species identification and
coral (Coles, 1996), and fish mortalities (Stirn cell counts, water samples (250 ml) were col-
et al., 1996). Cochlodinium polykrikoides has lected and preserved with 2% Lugol’s iodine
increased globally, not only observed in tropical solution. After one month, samples were allowed
systems (Stedeinger and Tangen, 1997), but also to settle and concentrate in 20-mm diameter
in temperate systems (Gobler et al., 2008; Mulhol- tubes. Prior to taxonomic analysis, samples were
land et al., 2009; Morse et al., 2011). C. polykri- further concentrated using a reverse filtration
koides blooms in the Sea of Oman and along the cone with 1 mm pore diameter nucleopore filter.
 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281 271
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Figure 1. Map of the coast of Oman and sampling site.

Cells were counted in a Nauman chamber (0.04– (Sorokin et al., 1975). Identification of harmful
0.75 ml) using light Olympus microscope. The species was based on Sournia (1986), Round
cell counts (N ml¡1) were determined using the et al. (1990), Hallegraeff et al. (2003), and
formula: N D (nK) where n is the abundance of Gomez et al. (2010). Seasons were classified as
cells of the given species in a sample; K is the Spring Intermonsoon (SIM) (April–June);
coefficient for the given sample. A coefficient K South–West summer Monsoon (SWM) (July–
was calculated for each sample: K D (Vs/Vc)/ September); Fall Intermonsoon (FIM) (Novem-
Vf, where Vs is sample volume; Vc is subsam- ber–December); North-East winter Monsoon
ple volume; Vf is the volume of filtered water (NEM) (January–March).
 272 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281
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Figure 2. Annual distribution of temperature ( C) in Bandar Khayran Bay (2006–2011).

Results Upwelling during SWM reduced the SST by about

4 C from its peak value during all sampling times,
The annual distribution of temperature showed except in 2008 when the SST dropped by 7 C.
a semi-annual cycle with peak temperatures being During the cooling phase of NEM, SST dropped to
recorded during SIM (April–June) and minimum about 23 C during the study period when the cool
temperatures during NEM (January–March) (Fig- penetrated to the bottom. The thermocline was
ure 2). Warming reached its maximum before the completely eroded during the winter cooling phase
start of SWM with the SST increasing to near with cool waters extending to bottom; during
30 C and above 32 C in 2007. Due to such intense SWM the thermocline raised towards surface
warming, the surface mixed layer was shallow. indicating upwelling event (Figure 2). Surface

Figure 3. Annual distribution of chlorophyll a (mgl¡1) in Bandar Khayran Bay (2006–2011).

 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281 273

chlorophyll a stayed below 1 mg l¡1 during most delicatula were present at lower concentrations
of the study (Figure 3). Chlorophyll a showed two (1500–6500 cells l¡1) at the same time. After
annual peaks: during the SWM and during the 2006, the populations of potentially harmful dia-
NEM when values ranged from 2–2.7 mg l¡1. The toms decreased significantly (Figure 5). Even
highest surface chlorophyll a (15.8 mg l¡1) during though potentially harmful dinoflagellates showed
this study was observed in 16 December 2008. dominance over diatoms in this study only three
Generally, nutrients showed increase in concen- taxa, Prorocentrum minimum, Scrippsiella tro-
trations during SWM and NEM seasons, while choidea and Noctiluca scintillans, appeared to be
SIM recorded the lowest concentrations (Fig- major constituents of the populations regularly
ure 4). Nitrate plus nitrite (NO3¡CNO2¡) concen- found in the water column. During this study mas-
trations remained below 2 mmol l¡1 during SIM sive blooms of Cochlodinium polykrikoides
seasons. Major peaks were observed during SWM occurred in Sea of Oman in November 2008, but
and NEM seasons (3–4.8 mmol l¡1). NEM 2006 the bloom progressed from the North West of the
recorded the highest NO3¡CNO2¡ concentrations Sea of Oman reaching the study area in early
in this study. Ammonia (NH4¡) showed an
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December 2008 (Figure 7). Because of the sam-

increase in concentration from 1 mmol l¡1 in pling schedule we had only two samples during
NEM 2007 to 5.8 mmol l¡1 in SWM 2007. Con- this bloom: December 2 and December 16 when
centrations remained between 2 and 3 mmol l¡1 the C. polykrikoides counts from the bloom were 8
during most of the study. SWM 2007 and 2011 £ 103 cells l¡1 (Chl a D 12.9 mg l¡1) and 210 £
recorded the highest concentrations of ammonia 103 cells l¡1 (Chl a D 15.3 mg l¡1), respectively.
(5.8 and 6 mmol l¡1), respectively. The seasonal During the next scheduled samplings 3 weeks
distribution of phosphate (PO4¡3) remained almost later, the bloom had already decayed, no cells of
stable with concentrations below 1 mmol l¡1 C. polykrikoides were found and Chl a dropped to
except during SWM 2007, NEM and SWM 2009 0.54 mg l¡1. However, continuous monitoring of
and FIM 2010 when concentrations rose above the bloom in the Muscat area was carried out at
1.5 mmol l¡1. Silicate (SiO2¡) concentration was several locations. Cochlodinium polykrikoides was
mostly above 1 mmol l¡1, but less than 2 mmol found to be significantly influenced by an increase
l¡1 except during SWM 2007 and NEM 2009 in nutrient concentrations and warmer than normal
when concentrations were 5.8 and 4.1 mmol l¡1, temperatures as well as the mixotrophic capabili-
respectively. ties of this species (Al-Azri et al., 2014).
Out of a total of 287 phytoplankton species The dinoflagellate Prorocentrum minimum and
encountered in this study, 24 species were identi- Scrippsiella trochoidea were observed throughout
fied as potentially harmful (Table 1). Dinoflagel- the sampling period (2006–2010) with higher
lates progressively increased reaching highest abundance at the depth of 1m compared to 10 m
abundance in 2008 when the Cochlodinium poly- (paired t-tests, p < 0.05) (Figure 7). The abundan-
krikoides bloom occurred (Figure 5). Following ces of these species were significantly higher dur-
that, harmful dinoflagellates decreased progres- ing SWM (August–September); this maximum
sively. Large fluctuations were observed in overall was particularly noticeable in late 2008 and early
dinoflagellate abundances ranging from 214 cells 2009 and coincided with massive blooms of
L¡1 to 16 £ 103 cells L¡1 and up to 200 £ 103 Cochlodinium polykrikoides. Prorocentrum mini-
cells l¡1 during the 2008 bloom. Overall, two mum started to increase in abundance during the
peaks of abundance were observed during the Cochlodinium blooms and reached a maximum of
study: a minor peak in NEM season and a major 14 £ 103 cells l¡1 after the decay of a bloom. The
peak in SWM (Figure 6). Potentially harmful dia- Scrippsiella trochoidea population was suppressed
toms were rare and were found only during fall of during the bloom event; however, an increase in
2006 at different concentrations (Figure 5). Lepto- abundance of S. trochoidea was observed after the
cylindrus minimus, Pseudo-nitzschia delicatissima decay of the bloom reaching a maximum of 13 £
and Pseudo-nitzschia pungens all proliferated dur- 103 cells l¡1 (Figure 7). Noctiluca scintillans
ing a short time period, in September 2006, exhib- formed massive blooms during fall and early win-
iting abundances of 64 £ 103, 51 £ 103 and 47 £ ter throughout the study except in 2008 and early
103 cells l¡1, respectively. Pseudo-nitzschia 2009 during the Cochlodinium polykrikoides
seriata, Cerataulina pelagica and Guinardia bloom (Figure 8). Dinophysis caudata, Dinophysis
 274 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281
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Figure 4. Seasonal fluctuations in concentrations of surface nutrients (mM) in Bandar Al-Khayran Bay.
 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281 275

Table 1. Potentially harmful phytoplankton species found in miles, Gonyaulax spinifera and Ceratium fusus
Bandar Khayran Bay. were rare and present only in a few months of the
year and in low numbers. Dinophysis caudata and
Potentially harmful Potentially harmful Gonyaulax spinifera were found only during
diatoms dinoflagellates SWM of 2006 and 2007, with higher abundances
Cerataulina pelagica Akashiwo sanguinea observed at 10 m compared to 1 m. Ceratium
Chaetoceros peruvianus Alexandrium fusus was rarely found during 2007, 2009 and
cohorticula 2010 and was more abundant at the surface during
Cylindrotheca Ceratium furca late SWM and early NEM of 2008.
closterium
Guinardia delicatula Ceratium fusus Discussion
Leptocylindrus minimus *Cochlodinium
polykrokiodes The assessment and early detection of alien
Pseudo-nitzschia Dinophysis acuminata species is a crucial step towards understanding and
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delicatissima mitigating the threat of invasive species in Oman

Pseudo-nitzschia Dinophysis caudata waters. In environments such as Sea of Oman and
pungens Arabian Sea with high traffic of oil tankers and the
Pseudo-nitzschia seriata Dinophysis miles lack of solid research of ballast water impact, we
Dinophysis mitra have used data of phytoplankton observation from
Gymnodinium our monitoring program as initial indication
catenatum assessment of threat of alien species. Most poten-
Karenia brevis tially harmful species encountered in this study
Lingulodinium showed a structural shift in their occurrence and
polyedrum dominance over the study period responding to
*
Noctiluca scintillans environmental conditions or bio-invasion. The
Phalacroma rotundatum abundance of the potentially harmful diatoms
Prorocentrum minimum Leptocylindrus minimus, Pseudo-nitzschia delica-
Scrippsiella trochoidea tissima and Pseudo-nitzschia pungens were
restricted to 2006 and increased in abundance dur-
*Bloom forming species in Oman waters. ing SWM seasons only, when the highest nitrogen
concentrations were observed and considerable

Figure 5. Yearly average counts of potentially harmful species in Bandar Khayran bay.
 276 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281
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Figure 6. Seasonal changes in potentially harmful dinoflagellates in Bandar Khayran Bay (2006–2011). Minus scale D 10 m
depth.

concentrations of silicate also occurred. This indi- of ballast waters in the Arabian Sea and Sea of
cated their need for high nutrient supplies in order Oman (personal communication, Regional Organi-
to proliferate and out-compete the dinoflagellates zation for the Protection of the Marine Environ-
that mostly dominate the phytoplankton assemb- ment ROPME) and the mixotrophic ability of this
lages in Bandar Khayran Bay (Al-Hashmi, 2012). species may have contributed to its rapid and sus-
Cochlodinium polykrikoides and Noctiluca scintil- tained growth during the period of low nutrient
lans were most abundant species. Scrippsiella tro- concentrations as mixotrophy was shown to dou-
choidea and Noctiluca scintillans were reported ble the growth rate of Cochlodinium polykrikoides
previously as common phytoplankton in Oman (Jeong et al., 2004). The coastal water of Oman
coastal waters (Thangaraja, 1990; Thangaraja lacks the baseline of indigenous species, and this,
et al., 2000; Al Gheilani, 2011). However, Proro- along with the lack of ballast water research, has
centrum minimum and Cochlodinium polykri- resulted in challenges in understanding the role
koides are reported for the first time. and impact of ballast water. Introduction of C. pol-
A devastating bloom of Cochlodinium polykri- ykrikoides in the region was attributed to ballast
koides appeared for the first time in Oman coastal water (Richlen et al. 2010; Al-Azri et al., 2014).
waters in November 2008, and covered the entire The bloom resulted in massive fish mortalities and
Arabian Gulf and Sea of Oman for more than huge economic losses (closed desalination plants,
10 months (Al Azri et al., 2014). Illegal discharge electric power stations and tourist sites); the
 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281 277
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Figure 7. Annual abundance of most common potentially harmful dinoflagellates in Bandar Khayran bay (2006–2011). Shading
corresponds to duration of Cochlodinium polykrikoides bloom in Bandar Khayran Bay.

C. polykrikoides blooms impact influenced the 2010) as well as in the Arabian Sea (Gomes,
component of the phytoplankton composition of 2009). The cell concentrations are higher during
the coastal water of Oman. Blooms of Noctiluca NEM than SWM, with some interannual variation
scintillans are a common yearly event in the Sea (Figure 8). In particular, these variations were pro-
of Oman (Al-Azri et al., 2007; Al-Hashmi et al., nounced in 2007 when the density of the bloom
 278 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281
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Figure 8. Annual abundance of Noctiluca scintillans Bandar Khayran bay (2006–2011). Shading corresponds to duration of
Cochlodinium polykrikoides bloom in Sea of Oman.

was highest, with the fall being the peak season been reported to survive in a wide range of envi-
(Figure 8). It is well documented that environmen- ronmental conditions (Tango et al., 2005) and
tal factors such as moderate rain fall, wind veloc- seems to compete significantly when there is low
ity, wind direction and advection of water masses concentrations of nitrate at the beginning of the
enhance the accumulation of N. scintillans leading bloom and when there is a high concentrations of
to bloom formation (Smayda, 1997; De la-Cruz the total nitrogen (Pertola et al., 2005). P. mini-
et al., 2003; Miyaguch et al., 2006; Al-Azri et al., mum has been described as an opportunist and a
2007). Noctiluca scintillans formed massive competitor in the phytoplankton community (Tas
blooms during fall and early winter throughout the and Okus, 2011) and has been reported to survive
study except in 2008 and early 2009 during the C. a wide range of temperature and salinity (Tango
polykrikoides bloom, presumably due to the allelo- et al., 2005) and its capability to utilize organic
pathic properties of C. polykrikoides. N. scintillans matter when inorganic nutrients are depleted
was not the only species affected by the presence (Jacobson and Anderson, 1993) has allowed P.
of C. polykrikoides blooms; S. trochoidea was also minimum to co-dominate other phytoplankton
affected due to allelopathic properties. However, communities (Heil et al., 2005). This may possibly
after the C. polykrikoides blooms, S. trochoidea be due to algal exudates affecting some species
increased in abundance, possibly due to a fast more than the others (Rice, 1984). Moreover, the
physiological adaptation in utilization of available community becomes more heterotrophic after the
nutrients and exudates produced during growth decay of a bloom, as organic nutrients are getting
and decomposition of the bloom (Linventon, released into the water (Riemann et al., 2000). P.
2001). minimum, the most persistent mixotrophic species
Unlike S. trochoidea, P. minimum was not in the bay, is favored by the supply of organic
greatly affected by the C. polykrikoides bloom. nutrients to grow and multiply (Carlsson et al.,
Instead, an increase in population was noticed and 1998, Glibert et al., 2001; Heil et al., 2005). Due
the maximum increase was reached after the decay to its small surface to volume ratio, P. minimum
of the C. polykrikoides bloom. P. minimum has has another advantage: its ability to take up
 Al-Azri et al. / Aquatic Ecosystem Health and Management 18 (2015) 269–281 279

nutrients even at very low concentration (Levin- Acknowledgements

ton, 2001; Olenina et al., 2010). In the current
study P. minimum showed changes in its abun- We acknowledge the support of the Department
dance during and after C. polykrikoides blooms. of Marine Science and Fisheries, Sultan Qaboos
High abundance during C. polykrikoides blooms University for the work reported here. We wish to
and after October 2009, the abundance of P. mini- extend our appreciation to Professor G. Halle-
mum and S. trochoidea were reduced to normal graeff for his review and constructive comments.
levels, probably due to a decrease in nutrient sup- Thanks to the crew of the Research Vessel Al
ply and recovery of grazers, as C. polykrikoides Jamiah.
causes strong mortality in zooplankton as well
(Jiang et al., 2009).
Phytoplankton species occurrence reported in Funding
our study showed either seasonal patterns or
responded to a major outbreak of phytoplankton This research is supported by the grants under
the projects RC/AGR/FISH/10/1 & IG/AGR/
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blooms. Their impact could have been relatively

short-term, but their long term impact could FISH/09/01 and U.S. National Science Foundation
extend to shifts in the phytoplankton component grant number OCE 082559.
and into other trophic levels.

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