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.

Introduction

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, agricultural activities and ballast water (Justic et al., 1995; Anderson et al., 2002; Sellner et al., 2003). In addition, natural processes such as water circulation, upwelling relaxation and cyst formation are also considered important factors contributing to formation of algal blooms (Levinton, 2001; Sellner et al., 2003). The introduction of non-indigenous marine phytoplankton species has been demonstrated to have considerable ecological and economic impacts especially in the coastal waters (Halleagraff, 1998; Richlen et al., 2010; Matsuoka et al., 2000). Unlike other marine invasive species, investigating the introduction of non-indigenous phytoplankton species and their impact in marine ecosystem poses substantial challenges. While some algae are known to produce toxins which 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) or gill clogging and damage due to mucus secretion and asphyxiation (MacLean, 1993; Rensel, 1993).

In the past several decades, massive expansion of both diatoms and dinoflagellate blooms has 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 blooms were not observed during the Joint Global Ocean Flux Study (JGOFS) cruises of the 1990s, but have expanded considerably except for diatoms blooms which showed a decline in a number of outbreaks. In general, diatoms blooms are dominated by Pseudo-nitzschia seriata, Climacodium frauenfeldianum and Guinardia flaccida species, although their occurrences were in low concentrations (Al-Hashmi et al., 2012). Unlike diatoms, dinoflagellate blooms have taken place in coastal areas since 1976, dominated by Ceratium furca, Karenia brevis and Noctiluca scintillans (Al-Gheilani et al., 2011). In 2000, Ceratium furca, Ceratium fusus and Karenia brevis have been reported to cause environmental impact and mass mortality of marine organisms in the coastal water of Oman (Thangaraja et al., 2000). Noctiluca scintillans appears responsible for more than 50% of HABs causing fish kills induced by oxygen depletion (Al-Azri et al., 2007; Al-Gheilani et al., 2011; Al-Azri et al., 2012). In Muscat coastal waters, blooms of N. scintillans are a seasonal event developing in early spring (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 in coral (Coles, 1996), and fish mortalities (Stirn et al., 1996). Cochlodinium polykrikoides has increased globally, not only observed in tropical systems (Stedeinger and Tangen, 1997), but also in temperate systems (Gobler et al., 2008; Mulholland et al., 2009; Morse et al., 2011). C. 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 (Richlen et al., 2010; Matsuoka et al., 2000). In view of these phenomena, it is important to monitor regional dynamics of HAB species and to investigate relationships between their occurrence and change in environmental conditions

The aim of this study was to investigate seasonal and interannual trends in the abundance of potentially harmful microalgae in the semi-enclosed Bay of Bandar Khayran in relation to environmental conditions and possible role of invasive species.

Methods

Despite the ephemeral nature of HABs and the large area to sample (3165 km of coastline, the Sea of Oman and the Arabian Sea), we have attempted to capture general trends in HABs by sampling bimonthly and during major bloom outbreaks. The bimonthly sampling was carried out at one station (BK) in the Bay of Bandar Khayran (Figure 1), at two depths (1 m and 10 m), from June 2006 to April 2011. Temperature, chlorophyll a and depth were measured with an Idronaut-Ocean Seven 316 CTD probe fitted with an additional sensor for chlorophyll a fluorescence. An initial CTD cast was performed, before taking water samples, to determine the depth profile and identify the mixed layer and thermocline position. Then, sub-surface water samples representative of the mixed layer were collected at 2 m 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 5-channel SKALAR FlowAccess auto-analyzer according to procedures described in Strickland and Parsons (1972) and modified by the manufacturer (Skalar Analytical, 1996).

Figure 1.

Map of the coast of Oman and sampling site.

Figure 1.

Map of the coast of Oman and sampling site.

For phytoplankton species identification and cell counts, water samples (250 ml) were collected and preserved with 2% Lugol's iodine solution. After one month, 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 with 1 µm pore diameter nucleopore filter. Cells were counted in a Nauman chamber (0.04–0.75 ml) using light Olympus microscope. 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; 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; Vf is the volume of filtered water (Sorokin et al., 1975). Identification of harmful species was based on Sournia (1986), Round et al. (1990), Hallegraeff et al. (2003), and Gomez et al. (2010). Seasons were classified as Spring Intermonsoon (SIM) (April–June); South–West summer Monsoon (SWM) (July–September); Fall Intermonsoon (FIM) (November–December); North-East winter Monsoon (NEM) (January–March).

Results

The annual distribution of temperature showed a semi-annual cycle with peak temperatures being recorded during SIM (April–June) and minimum temperatures during NEM (January–March) (Figure 2). Warming reached its maximum before the start of SWM with the SST increasing to near 30°C and above 32°C in 2007. Due to such intense warming, the surface mixed layer was shallow. Upwelling during SWM reduced the SST by about 4°C from its peak value during all sampling times, except in 2008 when the SST dropped by 7°C. During the cooling phase of NEM, SST dropped to about 23°C during the study period when the cool penetrated to the bottom. The thermocline was completely eroded during the winter cooling phase with cool waters extending to bottom; during SWM the thermocline raised towards surface indicating upwelling event (Figure 2). Surface chlorophyll a stayed below 1 μg l−1 during most of the study (Figure 3). Chlorophyll a showed two annual peaks: during the SWM and during the NEM when values ranged from 2–2.7 μg l−1. The highest surface chlorophyll a (15.8 μg l−1) during this study was observed in 16 December 2008.

Figure 2.

Annual distribution of temperature (°C) in Bandar Khayran Bay (2006–2011).

Figure 2.

Annual distribution of temperature (°C) in Bandar Khayran Bay (2006–2011).

Figure 3.

Annual distribution of chlorophyll a (μgl−1) in Bandar Khayran Bay (2006–2011).

Figure 3.

Annual distribution of chlorophyll a (μgl−1) in Bandar Khayran Bay (2006–2011).

Generally, nutrients showed increase in concentrations during SWM and NEM seasons, while SIM recorded the lowest concentrations (Figure 4). Nitrate plus nitrite (NO3+NO2) concentrations remained below 2 μmol l−1 during SIM seasons. Major peaks were observed during SWM and NEM seasons (3–4.8 μmol l−1). NEM 2006 recorded the highest NO3+NO2 concentrations in this study. Ammonia (NH4) showed an increase in concentration from 1 μmol l−1 in NEM 2007 to 5.8 μmol l−1 in SWM 2007. Concentrations remained between 2 and 3 μmol l−1 during most of the study. SWM 2007 and 2011 recorded the highest concentrations of ammonia (5.8 and 6 μmol l−1), respectively. The seasonal distribution of phosphate (PO4−3) remained almost stable with concentrations below 1 μmol l−1 except during SWM 2007, NEM and SWM 2009 and FIM 2010 when concentrations rose above 1.5 μmol l−1. Silicate (SiO2) concentration was mostly above 1 μmol l−1, but less than 2 μmol l−1 except during SWM 2007 and NEM 2009 when concentrations were 5.8 and 4.1 μmol l−1, respectively.

Figure 4.

Seasonal fluctuations in concentrations of surface nutrients (μM) in Bandar Al-Khayran Bay.

Figure 4.

Seasonal fluctuations in concentrations of surface nutrients (μM) in Bandar Al-Khayran Bay.

Out of a total of 287 phytoplankton species encountered in this study, 24 species were identified as potentially harmful (Table 1). Dinoflagellates progressively increased reaching highest abundance in 2008 when the Cochlodinium polykrikoides bloom occurred (Figure 5). Following that, harmful dinoflagellates decreased progressively. Large fluctuations were observed in overall dinoflagellate abundances ranging from 214 cells L−1 to 16 × 103 cells L−1 and up to 200 × 103 cells l−1 during the 2008 bloom. Overall, two peaks of abundance were observed during the study: a minor peak in NEM season and a major peak in SWM (Figure 6). Potentially harmful diatoms were rare and were found only during fall of 2006 at different concentrations (Figure 5). Leptocylindrus minimus, Pseudo-nitzschia delicatissima and Pseudo-nitzschia pungens all proliferated during a short time period, in 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) at the same time. After 2006, the populations of potentially harmful diatoms decreased significantly (Figure 5). Even though potentially harmful dinoflagellates showed dominance over diatoms in this study only three taxa, Prorocentrum minimum, Scrippsiella trochoidea and Noctiluca scintillans, appeared to be major constituents of the populations regularly found in the water column. During this study massive blooms of Cochlodinium polykrikoides occurred in Sea of Oman in November 2008, but the bloom progressed from the North West of the Sea of Oman reaching the study area in early December 2008 (Figure 7). Because of the sampling schedule we had only two samples during this bloom: December 2 and December 16 when the C. polykrikoides counts from the bloom were 8 × 103 cells l−1 (Chl a = 12.9 μg l−1) and 210 × 103 cells l−1 (Chl a = 15.3 μg l−1), respectively. During the next scheduled samplings 3 weeks later, the bloom had already decayed, no cells of C. polykrikoides were found and Chl a dropped to 0.54 μg l−1. However, continuous monitoring of the bloom in the Muscat area was carried out at several locations. Cochlodinium polykrikoides was found to be significantly influenced by an increase in nutrient concentrations and warmer than normal temperatures as well as the mixotrophic capabilities of this species (Al-Azri et al., 2014).

Figure 5.

Yearly average counts of potentially harmful species in Bandar Khayran bay.

Figure 5.

Yearly average counts of potentially harmful species in Bandar Khayran bay.

Figure 6.

Seasonal changes in potentially harmful dinoflagellates in Bandar Khayran Bay (2006–2011). Minus scale = 10 m depth.

Figure 6.

Seasonal changes in potentially harmful dinoflagellates in Bandar Khayran Bay (2006–2011). Minus scale = 10 m depth.

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.

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.

Table 1.

Potentially harmful phytoplankton species found in Bandar Khayran Bay.

Potentially harmful diatomsPotentially harmful dinoflagellates
Cerataulina pelagica Akashiwo sanguinea 
Chaetoceros peruvianus Alexandrium cohorticula 
Cylindrotheca closterium Ceratium furca 
Guinardia delicatula Ceratium fusus 
Leptocylindrus minimus *Cochlodinium polykrokiodes 
Pseudo-nitzschia delicatissima Dinophysis acuminata 
Pseudo-nitzschia pungens Dinophysis caudata 
Pseudo-nitzschia seriata Dinophysis miles 
 Dinophysis mitra 
 Gymnodinium catenatum 
 Karenia brevis 
 Lingulodinium polyedrum 
 *Noctiluca scintillans 
 Phalacroma rotundatum 
 Prorocentrum minimum 
 Scrippsiella trochoidea 
Potentially harmful diatomsPotentially harmful dinoflagellates
Cerataulina pelagica Akashiwo sanguinea 
Chaetoceros peruvianus Alexandrium cohorticula 
Cylindrotheca closterium Ceratium furca 
Guinardia delicatula Ceratium fusus 
Leptocylindrus minimus *Cochlodinium polykrokiodes 
Pseudo-nitzschia delicatissima Dinophysis acuminata 
Pseudo-nitzschia pungens Dinophysis caudata 
Pseudo-nitzschia seriata Dinophysis miles 
 Dinophysis mitra 
 Gymnodinium catenatum 
 Karenia brevis 
 Lingulodinium polyedrum 
 *Noctiluca scintillans 
 Phalacroma rotundatum 
 Prorocentrum minimum 
 Scrippsiella trochoidea 
*

Bloom forming species in Oman waters.

The dinoflagellate Prorocentrum minimum and Scrippsiella trochoidea were observed throughout the sampling period (2006–2010) with higher abundance at the depth of 1m compared to 10 m (paired t-tests, p < 0.05) (Figure 7). The abundances of these species were significantly higher during SWM (August–September); this maximum was particularly noticeable in late 2008 and early 2009 and coincided with massive blooms of Cochlodinium polykrikoides. Prorocentrum minimum started to increase in abundance during the Cochlodinium blooms and reached a maximum of 14 × 103 cells l−1 after the decay of a bloom. The Scrippsiella trochoidea population was suppressed during the bloom event; however, an increase in abundance of S. trochoidea was observed after the decay of the bloom reaching a maximum of 13 × 103 cells l−1 (Figure 7). Noctiluca scintillans formed massive blooms during fall and early winter throughout the study except in 2008 and early 2009 during the Cochlodinium polykrikoides bloom (Figure 8). Dinophysis caudata, Dinophysis miles, Gonyaulax spinifera and Ceratium fusus were rare and present only in a few months of the year and in low numbers. Dinophysis caudata and Gonyaulax spinifera were found only during SWM of 2006 and 2007, with higher abundances observed at 10 m compared to 1 m. Ceratium fusus was rarely found during 2007, 2009 and 2010 and was more abundant at the surface during late SWM and early NEM of 2008.

Figure 8.

Annual abundance of Noctiluca scintillans Bandar Khayran bay (2006–2011). Shading corresponds to duration of Cochlodinium polykrikoides bloom in Sea of Oman.

Figure 8.

Annual abundance of Noctiluca scintillans Bandar Khayran bay (2006–2011). Shading corresponds to duration of Cochlodinium polykrikoides bloom in Sea of Oman.

Discussion

The assessment and early detection of alien species is a crucial step towards understanding and mitigating the threat of invasive species in Oman waters. In environments such as Sea of Oman and Arabian Sea with high traffic of oil tankers and the lack of solid research of ballast water impact, we have used data of phytoplankton observation from our monitoring program as initial indication assessment of threat of alien species. Most potentially harmful species encountered in this study showed a structural shift in their occurrence and dominance over the study period responding to environmental conditions or bio-invasion. The abundance of the potentially harmful diatoms Leptocylindrus minimus, Pseudo-nitzschia delicatissima and Pseudo-nitzschia pungens were restricted to 2006 and increased in abundance during SWM seasons only, when the highest nitrogen concentrations were observed and considerable concentrations of silicate also occurred. This indicated their need for high nutrient supplies in order to proliferate and out-compete the dinoflagellates that mostly dominate the phytoplankton assemblages in Bandar Khayran Bay (Al-Hashmi, 2012). Cochlodinium polykrikoides and Noctiluca scintillans were most abundant species. Scrippsiella trochoidea and Noctiluca scintillans were reported previously as common phytoplankton in Oman coastal waters (Thangaraja, 1990; Thangaraja et al., 2000; Al Gheilani, 2011). However, Prorocentrum minimum and Cochlodinium polykrikoides are reported for the first time.

A devastating bloom of Cochlodinium polykrikoides appeared for the first time in Oman coastal waters in November 2008, and covered the entire Arabian Gulf and Sea of Oman for more than 10 months (Al Azri et al., 2014). Illegal discharge of ballast waters in the Arabian Sea and Sea of Oman (personal communication, Regional Organization for the Protection of the Marine Environment ROPME) and the mixotrophic ability of this species may have contributed to its rapid and sustained growth during the period of low nutrient concentrations as mixotrophy was shown to double the growth rate of Cochlodinium polykrikoides (Jeong et al., 2004). The coastal water of Oman lacks the baseline of indigenous species, and this, along with the lack of ballast water research, has resulted in challenges in understanding the role and impact of ballast water. Introduction of C. polykrikoides in the region was attributed to ballast water (Richlen et al. 2010; Al-Azri et al., 2014). The bloom resulted in massive fish mortalities and huge economic losses (closed desalination plants, electric power stations and tourist sites); the C. polykrikoides blooms impact influenced the component of the phytoplankton composition of the coastal water of Oman. Blooms of Noctiluca scintillans are a common yearly event in the Sea of Oman (Al-Azri et al., 2007; Al-Hashmi et al., 2010) as well as in the Arabian Sea (Gomes, 2009). The cell concentrations are higher during NEM than SWM, with some interannual variation (Figure 8). In particular, these variations were pronounced in 2007 when the density of the bloom was highest, with the fall being the peak season (Figure 8). It is well documented that environmental factors such as moderate rain fall, wind velocity, wind direction and advection of water masses enhance the accumulation of N. scintillans leading to bloom formation (Smayda, 1997; De la-Cruz et al., 2003; Miyaguch et al., 2006; Al-Azri et al., 2007). Noctiluca scintillans formed massive blooms during fall and early winter throughout the study except in 2008 and early 2009 during the C. polykrikoides bloom, presumably due to the allelopathic properties of C. polykrikoides. N. scintillans was not the only species affected by the presence of C. polykrikoides blooms; S. trochoidea was also affected due to allelopathic properties. However, after the C. polykrikoides blooms, S. trochoidea increased in abundance, possibly due to a fast physiological adaptation in utilization of available nutrients and exudates produced during growth and decomposition of the bloom (Linventon, 2001).

Unlike S. trochoidea, P. minimum was not greatly affected by the C. polykrikoides bloom. Instead, an increase in population was noticed and the maximum increase was reached after the decay of the C. polykrikoides bloom. P. minimum has been reported to survive in a wide range of environmental conditions (Tango et al., 2005) and seems to compete significantly when there is low concentrations of nitrate at the beginning of the bloom and when there is a high concentrations of the total nitrogen (Pertola et al., 2005). P. minimum has been described as an opportunist and a competitor in the phytoplankton community (Tas and Okus, 2011) and has been reported to survive a wide range of temperature and salinity (Tango et al., 2005) and its capability to utilize organic matter when inorganic nutrients are depleted (Jacobson and Anderson, 1993) has allowed P. minimum to co-dominate other phytoplankton communities (Heil et al., 2005). This may possibly be due to algal exudates affecting some species more than the others (Rice, 1984). Moreover, the community becomes more heterotrophic after the decay of a bloom, as organic nutrients are getting released into the water (Riemann et al., 2000). P. minimum, the most persistent mixotrophic species in the bay, is favored by the supply of organic nutrients to grow and multiply (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; Olenina et al., 2010). In the current study P. minimum showed changes in its abundance during and after C. polykrikoides blooms. High abundance during C. polykrikoides blooms and after October 2009, the abundance of P. minimum and S. trochoidea were reduced to normal levels, probably due to a decrease in nutrient supply and recovery of grazers, as C. polykrikoides causes strong mortality in zooplankton as well (Jiang et al., 2009).

Phytoplankton species occurrence reported in our study showed either seasonal patterns or responded to a major outbreak of phytoplankton blooms. Their impact could have been relatively short-term, but their long term impact could extend to shifts in the phytoplankton component and into other trophic levels.

Conclusions

The annual proliferation of the dinoflagellate N. scintillans bloom, along with the persistence of P. minimum and S. trochoidea throughout the annual cycle in higher abundances than other phytoplankton species, might indicate that these species have established local populations, which in turn enhances their capability to bloom under favorable conditions. The outbreak of C. polykrikoides in 2008 and 2009 might indicate the role of ballast water in introducing invasive species in the coastal water of Oman and response of the different phytoplankton groups to environmental changes.

We acknowledge that the best method of assessing the introduction and impact of alien species requires a long term monitoring program, which is lacking. It should be emphasized that using data from our routine monitoring program is a first step to assess impact of alien species in Omani waters. Our study reported major outbreaks of phytoplankton species and their impact on the shift of other groups; however, an interdisciplinary approach taking into account environmental changes to monitor the distribution and abundance of potentially HAB species will facilitate a comprehensive understanding and assessment of alien species. Furthermore, fundamental data about ship traffic, their ballast content and their discharge in Omani waters is lacking.

Acknowledgements

We acknowledge the support of the Department of Marine Science and Fisheries, Sultan Qaboos University for the work reported here. We wish to extend our appreciation to Professor G. Hallegraeff for his review and constructive comments. Thanks to the crew of the Research Vessel Al Jamiah.

Funding

This research is supported by the grants under the projects RC/AGR/FISH/10/1 & IG/AGR/FISH/09/01 and U.S. National Science Foundation grant number OCE 082559.

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