Marine Life Mortalities and Harmful Algal Blooms in the Northern Arabian Gulf Ã Faiza Y

Marine life mortalities and Harmful Algal Blooms in the Northern Arabian Gulf Ã Faiza Y. Al-Yamani, Igor Polikarpov, and Maria Saburova Ecosystem-Based Management of Marine Resources Program, Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, P.O. BOX 1638, Salmiya 22017, Kuwait Ã Corresponding author: [email protected]

Kuwait, which is located in the northwestern Arabian Gulf, has experienced several incidences of marine life mortality during the past two decades. Mortalities included pelagic and benthic fish, Sea Cucumbers and Mollusks including pearl oysters. Most of the mortalities occurred in Kuwait Bay, which is shallow and semi-enclosed. The Bay encompasses Sulaibikhat Bay, whose coastal waters are nutrient-rich and eutrophicated due to sewage discharge into its waters. Other mortalities were reported outside Kuwait Bay, especially in marinas and southern waters of Kuwait. Kuwait’s marine environment has been increasingly affected by harmful algal blooms, which increased by frequency and severity. Other Gulf countries experienced serious mortality incidences as well. Different causes were responsible for the different marine mortalities in Kuwait and the region, including untreated sewage input, eutrophication, bacterial infection, algal blooms, hypoxic conditions, pollution, and dredging. The above mortalities impacted the economy, and affected aquaculture activities, the fishing operations, coastal tourism, damaged coral reefs, and forced the closure of desalination plants. This study summarizes the different mortality incidents that occurred in the northwestern Arabian Gulf during the period of 1999 to 2019 and their possible causes. Efforts, taken by Kuwait to improve the environmental conditions of the degraded coastal area of Kuwait Bay, include for example, the desig- nation of a marine protected area in southern Kuwait Bay that would ensure the continued production of ecological services of the protected Bay area.

Keywords: fish kill, northwestern Indian Ocean, phytoplankton

Introduction of 239,000 km2, with a total volume of 7000- 8400 km3 (Emery, 1956; Purser and Seibold, The Arabian Gulf (referred to here as the Gulf), 1973; El-Gindy and Hegazi, 1996; Kampf and which is also referred to as the Persian Gulf or Sadrinasab, 2006). The Gulf is a marginal sea in Inner Sea of the ROPME Sea Area, is an arm of an arid zone, with a sub-tropical climate, mostly the Indian Ocean. It is a relatively shallow sea surrounded by deserts. It has an average rainfall of with a mean water depth of 35 m, with depths < 5 cm in coastal Arabia (Al-Yamani et al., 2004). exceeding 100 m occurring only at the Strait of The main freshwater inflow is from the Shatt Al- Hormuz. Extensive shallow regions < 20 m deep, Arab River, which forms at Qurna where the are found off the coasts of Kuwait, Bahrain, and Tigris and Euphrates Rivers join together and is the United Arab Emirates. The Gulf covers an area joined downward by the Karun River before it

196

Aquatic Ecosystem Health & Management, 23(2):196–209, 2020. Copyright # 2020 AEHMS. ISSN: 1463-4988 print / 1539-4077 online DOI: 10.1080/14634988.2020.1798157

Downloaded from http://read.dukeupress.edu/aehm/article-pdf/23/2/196/899272/196al-yamani.pdf by guest on 29 September 2021 Al-Yamani et al. / Aquatic Ecosystem Health and Management 23 (2020) 196–209 197

discharges into the northern Gulf (Al-Muhyi, industry, and overfishing) and their impacts on 2015). The mean surface salinity of the Gulf is the Gulf’s marine systems. about 41 psu. High salinities of the Gulf are due to This study summarizes a range of incidents of high evaporation rates, which exceed the sum of marine biota mortality in the northwestern Gulf precipitation with an annual mean of 34 km3 and since the first fish kill reported in Kuwait’s river discharge with an annual mean of 37 km3 waters in 1999 to date, and their possible causes. (Al-Yamani et al., 2004; Sheppard et al., 2010). Mean evaporative water losses are estimated to be about 326 km3 per year (Sheppard et al., 2010). Marine life mortality incidences The Gulf is connected to the Sea of Oman and the in the northwestern Gulf (a case Arabian Sea through the Strait of Hormuz, where study in Kuwait’s waters) water exchange between the Gulf and the Sea of Oman occurs. More water of about 3365 km3 Kuwait’s waters in the northwestern Gulf are À year 1 flows into the Gulf than exits the Gulf shallow with a maximum depth of about 30 m, À (3110 km3 year 1) through the Strait of Hormuz well-mixed, and biologically rich. The seawater (Ackleson et al., 1992). temperature ranges from 10 Cto36C, and has a The general circulation of the Gulf is counter- mean salinity of 42 psu (Al-Yamani et al., 2004). clockwise, and is mainly driven by halocline However, surface salinity varies in Kuwait’s forces caused by the high evaporation rates waters due to the seasonal and interannual fluctua- (Reynolds, 1993). The northwesterly or “shamal” tions in the discharge volume of Shatt Al-Arab wind plays an important role in the large-scale cir- (Al-Yamani et al., 2004; Al-Said et al. 2019), culation of the Gulf (Perrone, 1979), and influence which is attributed to human intervention in river- the coastal currents and storm surges, especially, ine flow upstream (Al-Yamani et al., 2017). in the southern basin (Cavalcante et al., 2016). Almost all of Kuwait’s coasts have been modi- In recent years, the marine environment of the fied, except part of the northern coast of Kuwait Gulf has been the focus of many studies, dealing Bay. Legal and illegal structures (>850 structures with its oceanographic characteristics, ecology, including boat ramps, small harbors, piers, jetties, biodiversity, biogeochemical processes, fisheries retaining walls and wave breakers, among others) and the impacts of natural as well as anthropogenic exist on Kuwait’s coast (Al-Mutairi et al., 2014; activities on its ecology and productivity (Hamza Devlin et al., 2015). Along Kuwait’s shores, hun- and Munawar, 2009; Nezlin et al., 2010; Sheppard dreds of hectares of land have been reclaimed and et al., 2010; Al-Yamani et al., 2012, 2017; dredged; however, even with these modifications, Polikarpov et al., 2016; Al-Said et al. 2019; Al- Kuwait’s coastal zone remains a productive com- Yamani and Naqvi, 2019; Devlin et al., 2019). ponent of the marine ecosystem (Al-Yamani et al., The extreme conditions of the Gulf, especially 2004; Sheppard et al., 2010). Probably, some of with regard to temperatures and the impact on the the artificial structures, such as marinas, can play a marine fauna, is driving a growing interest in positive role for marine life by increasing of diver- conducting studies with a focus on the potential sification of underwater coastal landscapes, pro- impact of climate change on the Gulf’s marine viding shelters and food for early life stages and environment and its biota (Burt et al., 2014; hard substrates for sessile marine organisms, Vaughan and Burt, 2016; Ben-Hassan and including bio-filtrators, such as sponges. Christensen, 2019). Kuwait has experienced several incidences of An up-to-date review of the current status of marine mortalities (Fig. 1), the causes of which are the Gulf’s marine environment and ecosystems, numerous and sometimes overlapping. Examples the threats to these valuable ecosystems, as well of the causes for the localized die-off of fish and as management efforts to rehabilitate and con- invertebrate populations are natural causes such as serve them is provided by Vaughan et al. (2018). hypoxia, as well as other causes such as infectious They addressed the subject of climate change as diseases and parasites, eutrophication and reduc- well as the different anthropogenic activities (e.g. tion in water quality (due to sewage discharges, coastal development, wastewater discharge, agricultural runoff, oil or hazardous waste spills), desalination plants, shipping traffic, petroleum reduced oxygen concentration in the water column

Downloaded from http://read.dukeupress.edu/aehm/article-pdf/23/2/196/899272/196al-yamani.pdf by guest on 29 September 2021 198 Al-Yamani et al. / Aquatic Ecosystem Health and Management 23 (2020) 196–209

and bottom, harmful and toxic algal blooms, 2002). Whether this dinoflagellate species was dredging affecting bottom biota, as well as some- ichthyotoxic or that the fish died from secondary times ‘unknown’ causes. The hypoxic event may harmful effects associated with that bloom still be brought on by factors such as algal blooms, remains uncertain, but it was decided that high temperatures, and thermal pollution. eutrophication of Kuwait Bay caused by elevated Fish kills associated with desalination plants nutrients, potentially from aquaculture activities due to thermal pollution and high concentration as well as industrial and untreated sewage inputs, of free chlorine were reported in 1995, 1996, could have caused the initiation and maintenance 1997 and 1998 in Kuwait. Fish mortality was of the Karenia bloom, which lead to fish mortal- also related to oil spill from the tanker in Kuwaiti ity in Kuwait Bay (Heil et al., 2001). waters in 1996 (Al-Yamani et al., 2000). Later, several other factors have been reported as rea- 2001 fish mortality associated sons for marine mortalities in Kuwait’s waters (Al-Yamani et al., 2012). The assessment of with bacterial infection long-term records of marine mortality in In August and September 2001, Kuwait Bay Kuwait’s waters is a challenge since, apart from experienced a massive kill of wild Klunzinger’s the two well-documented fish kill reports in 1999 mullet Liza klunzingeri that resulted in over 2,500 and 2001 in peer reviewed literature (Heil et al., tons of dead fish (Glibert et al., 2002). This event 2001; Glibert et al., 2002), published details are was nearly 100-fold larger than the previous major very sparse and not sufficiently documented. fish kill of 1999 in this region, which was associ- Unfortunately, most of the marine mortality ated with red tide (Heil et al., 2001). reports from the region do not include mortality In early August 2001, dead cultured European estimates of the affected species nor estimates of gilthead seabream Sparus aurata were observed in economic loss, which are of high importance. the aquaculture cages. The numbers of dead fish Below the reports of notable mortality incidents ’ per cage per day ranged from roughly 100 to over in Kuwait s marine environment are listed and 1000 by the end of the first week of August. supported by available details including photo- Coincident with this fish kill was the observation graphs, identification of affected species, meas- of a significant bloom of the dinoflagellate urements of concurrent environmental variables Ceratium furca near the cages site. By mid to late and water quality assessments, and mortality August, the dinoflagellate bloom had dissipated, magnitudes whenever possible. and the sea bream mortalities in the fish cages were reduced. Concurrently, dead wild mullets 1999 fish mortality and first were observed in Kuwait Bay. As the fish kill pro- gressed over the following days to weeks, dead potentially toxic algal and dying mullets were continually observed, in bloom incident addition to other species of dead and dying fish. These other species, however, represented a minor The first recognized potentially toxic algal fraction of the total dead fish, less than 5% bloom in Kuwait’s waters was caused by the (Glibert et al. 2002; Al-Marzouk et al., 2005). dinoflagellate Karenia selliformis, previously The massive fish mortality in August- identified as Gymnodinium sp. (Heil et al., 2001). September 2001 in Kuwait Bay was attributed This bloom occurred during September and to bacterial disease outbreak (Streptococcus October 1999 with an extensive and massive agalactiae) rather than to the impact of algal mortality (25 to 30 tons of dead fish) of wild toxins, despite the presence of paralytic shellfish largescale mullets Planiliza macrolepis, together poisoning-related dinoflagellates Gymnodinium with mortality of approximately 80,000 fish of catenatum and Pyrodinium bahamense as well as farmed sobaity (seabream Sparidentex hasta)in non-toxic bloom-forming dinoflagellates C. furca mariculture floating cages in Kuwait Bay (Heil and Gymnodinium impudicum, which were found et al., 2001). The above incident lead to substan- in the fish kill area (Glibert et al., 2002). tial economic losses for Kuwait estimated to be The bacterium S. agalactiae was implicated as about 7 million U.S. dollars (Al-Yamani et al., the primary cause of the wild fish kill in Kuwait

Fig. 1. Marine mortality evidences in Kuwait’s marine environment during 2005-2019: (A) satellite image (Google Earth) of Kuwait’s marine area with marine mortality sites (Catfish – orange circles; Sardinellas – red circles; Sea Cucumbers – blue circle; Mollusks – pink circle); dead Catfish (B) and Sardinellas (C) on the surface of Kuwait’s waters; dead Sea Cucumbers (D) and Pearl Oysters Pinctada radiata and Scallops Chlamys livida (E) washed ashore along Kuwait’s southern shores.

bay in 2001 (Evans et al., 2002). Streptococcosis interaction between the fish, the pathogens, and is a well-known, global distributed disease affect- the marine environment. It is also a function of ing both cultured and wild fish. Transmission of the vulnerability of the fish to pathogen infection agents is considered to be a complex (Shoemaker et al., 2001). It was reported that

Downloaded from http://read.dukeupress.edu/aehm/article-pdf/23/2/196/899272/196al-yamani.pdf by guest on 29 September 2021 200 Al-Yamani et al. / Aquatic Ecosystem Health and Management 23 (2020) 196–209

dead fish were rapidly scavenged by smaller fish 2011 summer fish mortalities in during the observed fish kill (Glibert et al., ’ 2002), but the extent to which bacteria were marinas along Kuwait s shores transmitted by this pathway is not known. Glibert The second series of massive fish kills in et al. (2002) hypothesized that the development Kuwait’s coastal waters occurred in several mari- and subsequent collapse of the dinoflagellate C. nas in Salmiya area and southwards during sum- furca bloom may have led to stressful conditions mer 2011 (Fig. 1 A, C). First reporting of fish that resulted in the initial fish kill in the maricul- kill incident was registered on June 5, 2011 at ture cages in early August 2001. Because seab- 16:00 in Ras Al-Ardh marina. Next day, about reams were possible carriers of the S. agalactiae, thousands of dead fish were observed in a nearby their death, their co-habitation with mullet, and Rescue Station marina (Fig. 2A). The kill con- the increased vulnerability of mullet to this sisted of mostly small specimens of Fringescale pathogen, may have led to the spread of this dis- Sardinella S. fimbriata, 10-12 cm long. Less ease (Glibert et al., 2002). Moreover, Jafar et al. intensive fish kills were observed also during 7-9 (2009) emphasized the possibility of sewage in June in several other marinas in the Salmiya area. Kuwait Bay being the source of infection for It was found that the in-situ DO concentrations fish. Majority of the isolates recovered from mul- in Ras Al-Ardh marina measured by a CTD pro- lets exhibited random amplification of poly- filer (JFE Advantech Co., Ltd., Japan) were 1.45 ml lÀ1 (1.93 mg lÀ1) on 1 m depth and morphic DNA patterns that were highly similar À1 À1 to those obtained from S. agalactiae recovered 0.08 ml l (0.11 mg l ) near bottom, with 35% and 1.80% of saturation, respectively at water tem- from sewage water, thereby implying their common origin (Jafar et al., 2009). Glibert et al. perature range of 29-30 C and salinity of 43 psu. (2002) suggested that nutrient enrichment pos- At the same day, in the nearby Marina Crescent concentration and saturation of oxygen were sibly due to sewage input into the coastal waters À À 4.84 ml l 1 (6.44 mg l 1) with 116.8% saturation was an important factor contributing to the 2001 À À at 1 m depth and 2.47 ml l 1 (3.29 mg l 1) with epizootic fish mortality. 58.8% saturation at the bottom. Hypoxic concentrations were observed for several days in several 2005 Sardinellas mortality in marinas along the shores south of Kuwait Bay. Chlorophyll-a concentrations ranged from ’ À marinas along Kuwait s coast 1.09-9.76 lgl 1 and the dominant phytoplankton In the morning of August 10, 2005, the sur- species in the fish kill area was small-sized chain- face of small semi-enclosed Ras Al-Ardh marina forming diatom Chaetoceros pseudocurvisetus (Fig. 3 E, F) with an average concentration of in Salmiya (Fig. 1A) was covered by dead À 2.0 ± 0.8 105 cells l 1, which constituted 49.2% of Fringescale Sardinella Sardinella fimbriata. The the total phytoplankton abundance. This diatom is surface area of water covered by Sardinellas was a common bloom-forming species which is estimated approximately to be over 0.07 hectares. observed in Kuwait’s waters (Al-Yamani et al., Due to high water temperature and low tide, it 2012). Fish pathology investigations have revealed was assumed that fish schools were probably no parasites or viruses in dead fish tissues, but trapped in the marina by predatory fish. During some Gram-negative bacteria (Vibrio sp.) were low tide the Sardinellas were asphyxiated because present that normally are expected to occur when of low dissolved oxygen concentrations in the the fish is under stress (Dr. Azad Ismail Saheb, seawater within the marina. Dissolved oxygen Kuwait Institute for Scientific Research (KISR), À1 (DO) concentrations were 1.8, 1.7 and 1.0 mg l Kuwait, pers. comm.). in surface, middle and bottom water depths. At Most fish cannot live below 30% oxygen sat- salinity of 40 psu and water temperature of uration. A "healthy" aquatic environment seldom 30 C, such DO concentrations equaled oxygen experiences less than 80% oxygen saturation. The saturation of 29.7, 28.0 and 16.5%, correspond- minimum dissolved oxygen requirements for ingly. All these values are hypoxic and lethal for tropical marine fish is a concentration of 5 mg most fish (Svobodova et al., 1993). lÀ1 (approximately 75% saturation). These values

Fig. 2. Fish kill in Salmiya and Messila areas in June-July 2011: (A) collection of dead fish in Rescue Station marina, Salmiya, July 19, 2011; (B, C) dead Sardinellas on the surface of Messila Palace marina, Messila, July 24, 2011; (D, E) light microscope images of bloom forming diatom Chaetoceros pseudocurvisetus in bright field (D) and fluorescent (E) illumination; (F) light microscope image of bloom-forming dinoflagellate Gonyaulax verior in bright field illumination; (G-I) vertical profiles of oceanographic variables in Rescue Station marina in Salmiya during fish kill incidents measured by oxygen sensor installed on JFE CTD sonde: (G) oxygen saturation on June 8, 2011; (H, I) dissolved oxygen concentration and water temperature on July 19, 2011

are minimum requirements for healthy growth, on the same dates and at same locations can be tissue repair and reproduction of fish (Svobodova characterized also as hypoxic, with saturation et al. 1993). ranging between 8.5% for Ras Al-Ardh and 0.5% Oxygen saturation data on 6-8 June, 2011 for for adjacent areas, which are considered lethal locations such as Ras Al-Ardh marina, and adja- levels for most fish and other marine animals. cent semi-closed areas indicated hypoxic condi- Vertical profile of oxygen saturation levels at the tion even at a depth of 1 m (surface layer) with Rescue Dock on 8 June, 2011 confirmed the the range of saturation level being between 35 abrupt decrease of oxygen saturation level at and 14.5%, which is a dangerous level for fish about 4 m of depth (Fig. 2G). Thus, at the mari- life and survival. Near-bottom saturation levels nas, a near-bottom dysaerobic zone was found at

Downloaded from http://read.dukeupress.edu/aehm/article-pdf/23/2/196/899272/196al-yamani.pdf by guest on 29 September 2021 202 Al-Yamani et al. / Aquatic Ecosystem Health and Management 23 (2020) 196–209

Fig. 3. Catfish kill along southern shore of Kuwait Bay in April 2017: (A) dead Catfish in inshore waters of Kuwait Bay; (B) vertical profile of oxygen concentration measured on April 30, 2017, at Sulaibikhat Port (the straight line marks the hypoxic oxygen concentration towards the bottom); (C-G) light and scanning electron micrographs of bloom-forming diatoms Thalassiosira concaviuscula (C, D) and Skeletonema grevillei (E-G); (H-I) histopathology of the gill tissue stained with hematoxylin and eosin stains from Catfish Netuma sp. collected in Shuwaikh on April 23, 2017, showing in (H) enlarged apical mucus cells (MuC), and in (I) chloride cells (CC) in the basement of secondary lamellae. B - courtesy Dr. Takahiro Yamamoto, KISR; H, J – courtesy Dr. Azad Ismail Saheb, KISR.

the boundary of anoxic and hypoxic zones, hypoxic condition in the Rescue Station marina where the life of all aerobic marine organisms (Fig. 2 H, I). Later, fish kill was registered during was under instant danger (Savrda and July 21-23 southwards in the Messila marina Bottjer, 1987). (Fig. 2 B, C), where DO concentration in surface The next significant fish kills of the same fish 1-m layer was 0.2 mg lÀ1. In addition, significant species, S. fimbriata, was observed in the bloom of the dinoflagellate Gonyaulax verior Salmiya area on July, 19, 2011. Along with fish (>106 cells lÀ1) causing water discoloration was mortality, water profiling showed the forming of revealed (Fig. 2F).

marina in large numbers, and with time, causing the oxygen level in the marina water to fall, contributing to their death.

Sporadic Catfish mortality in Kuwait Bay Catfish is a benthic fish that occurs in high abundance in Kuwait Bay. Catfish mortality was reported in Kuwait Bay in 2006, 2015, 2017 and 2019, especially during late spring and early summer (April, May and June). Evidence of red tide and most significant Catfish mortality were Fig. 4. Frequency of algal bloom events in Kuwait’s marine recorded within the inshore waters of Kuwait environment during 1988-2017 summarized within five-year Bay in April-May 2017 (Fig. 3A). The extent of intervals; algal bloom events are indicated by red when were the fish kill area in southern Kuwait Bay was associated with fish mortality (fish mortality event was considered if more than 100 dead fish were observed along 100 m from Kuwait Towers to Doha and Eshairij. The of coast or in marina) (source; Al-Yamani and Environment Public Authority (EPA) of Kuwait Saburova, 2019). and the Public Authority of Agriculture and Fisheries Resources (PAAFR) reported about 60 tons of dead Catfish collected from the shores of Kuwait Bay during April and early May 2017 The increase of organic carbon content due to (KUNA, 2017). Two species of Catfish, Netuma the die-off phase of phytoplankton blooms, and thalassina and Policofollis tenuspinus, were water stratification in semi-enclosed marinas ’ involved in the fish kill. The fish were found along Kuwait s shore coincided with the observed dead or in morbid condition (Fig. 1 A, B; 3A). In oxygen depletion, which might have led to local addition, some morbid and dead mullets L. klun- fish kills during June-July 2011. The probable zingeri were also reported later in April in scenario of fish kill included high organic load Kuwait Bay. (from municipal sewage and decaying algal DO concentrations in the coastal waters of bloom), with lack of wind and limited water mix- Sulaibikhat Bay off Shuwaikh were moderate to ing coupled with warm summer temperature and high during day-time sampling, with highest con- moderate humidity, contributed to the low oxy- centration of 11.69 mg lÀ1 recorded on April 12, gen concentrations in the water column and, par- 2017, and the lowest concentration of 3.28 mg ticularly the bottom layer in semi-enclosed lÀ1 recorded toward the bottom on April 23. In marinas, and hence resulted in mortality of fact, over two-thirds of the day-time measure- schooling Sardines. Fish kills in marinas have ments yielded DO exceeding 5 mg lÀ1. Hence, been reported elsewhere in the Gulf, such as the the oxygen levels were well above the threshold latest incident in Muscat, Oman in October 2019. level of hypoxia (2 mg O2 per liter or lower) Dr. Sergey Dobretsov from Sultan Qaboos known to significantly impact marine life University reported that ardines fish had perished (Vaquer-Sunyer and Duarte, 2008). However, because of a lack of oxygen in the water at night- hypoxic (DO < 2mg lÀ1) and even anoxic (DO time. Sardines are schooling fish, active and < 0.5 mg lÀ1) conditions were encountered by move in large numbers, and require large CTD profiling in the Shuwaikh Port area on amounts of oxygen, which was not available at April 30, 2017. Hypoxia was found at a depth of night time in the shallow marina waters (Times 10 m, and anoxic conditions were found at the of Oman, 2019). Another reason was proposed bottom (10.6 m), while surface DO, were even by Mr. Ahmed Al Mashani, in the same news- higher than 9 mg lÀ1 (Fig. 3B). paper report, stating that the kill occurred when Histopathology examination revealed no bac- large predator fishes chased Sardines, leading terial pathology but showed the gills to be them to enter and get trapped into the shallow inflamed (Dr. Azad Ismail Saheb, KISR, Kuwait,

Downloaded from http://read.dukeupress.edu/aehm/article-pdf/23/2/196/899272/196al-yamani.pdf by guest on 29 September 2021 204 Al-Yamani et al. / Aquatic Ecosystem Health and Management 23 (2020) 196–209

pers. comm.). Microscopic investigations of saturation levels (Svobodova et al., 1993), and Catfish gills detected hypertrophied lamellar epi- this factor could also contribute to fish mortality. thelial cells and ballooning of the lamellar epithe- lium. Enlarged mucus cells, especially, those at the tips of the secondary lamellae and enlarge- ment of the chloride cells indicated stress-medi- ated response (Fig. 3 H, I). Excess production of 2013 massive Mollusks mortality mucus which in turn blocks the respiratory sur- in Khiran face could result in a state of hypoxia for the fish, not related to the dissolved oxygen levels in Massive mortality of the pearl oyster Pinctada seawater at the time of fish mortality. radiata and scallop Chlamys livida, was recorded High biomass phytoplankton blooms associ- in the Khiran area along Kuwait’s southern shore ated with Catfish mortality were recorded along in October and November 2013 (Fig. 1A, E). the southern shore of Kuwait Bay in Shuwaikh Numerous valves of the dead Mollusks washed and Sulaibikhat Bay in June 2015, April-May out onto the Khiran shore (Fig. 1E). Along with 2017, and May 2019. Although the total phyto- Mollusks mortality, a few dead Crabs, Sea plankton abundance varied significantly within Cucumbers, and fish were observed in the the areas associated with fish mortality among same area. 6 8 À1 the years (1.8 10 – 5.8 10 cells l ), the Phytoplankton or microphytobenthic blooms observed phytoplankton composition was almost were not detected in the Khiran area, suggesting identical with respect to the dominant species. that the observed Mollusk’s mortality event was Phytoplankton within the areas associated with not linked to a microalgal bloom and the mortality fish mortality in 2015, 2017 and 2019 was found was likely caused by other factors, and most prob- to be strongly diatom-dominated. The small-sized ably by the intensive dredging activities of the chain-forming centric diatoms Thalassiosira spp. nearby mega Khiran residential/chalet project, and Skeletonema grevillei (Fig. 3 C-G) as well as especially that dredging occurred in the proximity the tiny pennate diatoms Nitzschia cf. laevis and of dense oyster beds in Khiran. Dredging increases Nitzschia pusilla dominated the phytoplankton suspended sediment loading in the water, causing numerically and jointly contributed more than either the direct burial of oyster beds or reductions 94-99% of the total phytoplankton abundance. in the filtration efficiency and respiration rates of The genus Thalassiosira was manifested in scan- the affected oysters (Wilber and Clarke, 2010). ning electron microscope as a diverse species Hence, dredging could have been a factor in the complex that included more than ten distinct Mollusks’ mortality. taxa. Among them, Thalassiosira concaviuscula Studies conducted by Al-Hashem and was found to be the most abundant and bloom- forming species (Fig. 3 C, D). Behbehani (2016) and Al-Hashem (2017) on adult The phytoplankton blooms were followed by pearl oyster P. radiata collected from the Khiran extensive fish mortality in Kuwait Bay that coast during the November 2013 mass mortality became especially serious in April 2017. The incidence indicated contamination by polycyclic mortality could have occurred due to one or more aromatic hydrocarbons (PAHs). The oyster sam- of the following factors: direct impact of pollu- ples displayed histopathological changes in gills as tion from sewage discharge, or hypoxia caused well as necrosis and edemas of branchial lamellae, by decay of organic matter produced by algae complete degeneration of gill filaments, loss of and/or sewage together with near-bottom sedi- regular shape and hemolysis, and inflammation. ment anoxia. The study by Al-Hashem and Behbehani (2016) Because mostly Catfish species mortality was reported the detection of PAHs in sea water, sedi- reported during this incident, it was presumed ment and oyster tissues, and concluded that the that the main reason could be near bottom oxy- PAHs-caused severe histopathological changes in gen depletion, especially during night-time. the gills of P. radiata and hence, could be one of Toxicity of dissolved ammonia (from discharged the reasons for the oyster mortality at Al-Khiran sewage) can significantly increase at low oxygen beach in November 2013.

2018 Sea Cucumber mortality at et al., 2002; Al-Yamani et al., 2004, 2012; Nezlin ’ et al., 2010; Polikarpov et al., 2009, 2016; Kuwait s southern shore Sheppard et al., 2010; Al-Yamani and Saburova, ’ An incident of Sea Cucumbers mortality was 2019). Microalgal blooms occur in Kuwait s recorded in December 2018 at Kuwait’s southern waters year round and are caused by proliferation shore near Mina Al-Shuaiba (Fig. 1A, D). A large of diatoms, dinoflagellates, cryptophytes, number of dead Sea Cucumbers, Holothuria are- prymnesiophytes, raphidophytes, chlorophytes, nicola, were washed ashore at the beach (Fig. cyanobacteria, and ciliates (Al-Kandari et al., 1D), many were dead while others were in a 2009; Al-Yamani et al., 2012, Al-Yamani and moribund state. The site where the mortality hap- Saburova, 2019). The first documented algal pened is a sandy beach interspersed with fossil- blooms in Kuwait’s waters were caused by the ized reefs and rocky outcrops near the littoral colonial prymnesiophyte algae Phaeocystis sp. zone. H. arenicola are mostly seen deeply buried (Al-Hassan et al., 1990), and the photosynthetic in the sand underneath the rocks and are active ciliate Myrionecta rubra (Subba Rao and Al- deposit feeders. No water discoloration or abnor- Yamani, 1998). Many other algal bloom events mal water odor were reported at the site. have been documented since then (Subba Rao However, storm water discharge of rain water to et al., 1999, 2003; Al-Yamani et al., 2000, 2012; the beach was noted. Al-Kandari et al., 2009; Al-Yamani and At the beach where dead holothurians were Saburova, 2019). found, both pelagic and benthic microalgae were Phytoplankton blooms were largely associated abundant. However, no potentially harmful with coastal waters along Kuwait’sshore,with microalgal species to marine invertebrates were Kuwait Bay experiencing most of the harmful algal recorded in the composition of the microalgal bloom (HAB) incidents. Diatom-dominated blooms assemblages. The abundance of the pelagic were recorded more frequent than other microalgal microalgal fraction was essentially dominated by groups and were most widely distributed across nanoflagellates. The small-sized cryptophycean Kuwait’s waters with high frequency of occurrence flagellates (aff. Plagioselmis prolonga) were the in Kuwait Bay. Dinoflagellate-, flagellate- and cili- most abundant and bloom-forming. The sand- ate-dominated bloom events were mainly restricted dwelling microalgal fraction was predominated to Kuwait Bay and adjacent coastal waters, whereas by naviculoid diatoms. rare cyanobacterium-dominated blooms were asso- The Sea Cucumbers were most likely stressed ciated with southern Kuwait’s waters exclusively. in situ by an unknown factor, washed up from Species belonging to the genera Chaetoceros, the bottom sediments, and then the affected Sea Nitzschia, Thalassiosira and Skeletonema were Cucumbers died and washed ashore. The most among the most commonly bloomed diatoms. plausible cause is that a sudden decline in salinity Karenia papilionacea was the most frequently from 45 to 5 psu in the nearshore waters occurred bloomed dinoflagellate species, and cryptophy- due to rainwater discharge from a rain water ceans, raphidophycean Heterosigma akashiwo and drain, which likely caused an osmotic shock to colonial haptophyte Phaeocystis globosa were most the Sea Cucumbers during the ebb tide, and led common bloom-forming flagellates. to their mortality. Many holothurians were Kuwait’s marine environment has been observed on the beach in a moribund state. increasingly affected by HABs (Fig. 4). Most of the algal blooms reported so far in Kuwait are Harmful Algal Bloom incidences harmless to human health, however, such blooms in Kuwait’s waters may have deleterious impact including the development of high biomass, leading to oxygen Seasonal phytoplankton blooms are part of the depletion, shading of submerged aquatic plants, annual succession in marine ecosystems and are alteration of food webs, and suffocation of fish typical phenomena in Kuwait’s waters as well as from mucus production and gill interference, in the Gulf region and the adjacent Sea of Oman leading to fish kills and other environmental and (e.g. Subba Rao and Al-Yamani, 1998; Jones economic outcomes (Subba Rao et al., 1999,

Downloaded from http://read.dukeupress.edu/aehm/article-pdf/23/2/196/899272/196al-yamani.pdf by guest on 29 September 2021 206 Al-Yamani et al. / Aquatic Ecosystem Health and Management 23 (2020) 196–209

2003; Al-Yamani et al., 2000, 2004, 2012; to isolates from the northeastern USA, Puerto Glibert, 2007; Al-Yamani and Saburova, 2019). Rico, Mexico, and Malaysia, known as the ‘‘American/Malaysian’’ ribotype (Richlen et al., 2010). Richlen et al. (2010) stated that the occur- Harmful Algal Blooms in the rence of C. polykrikoides in the Gulf waters was Gulf and Sea of Oman due to the global expansion of this taxon possibly by the introduction of this species through ballast Over the past decades, the occurrence of algal water discharge. Recent increase in HAB impacts blooms has increased both in frequency and observed in this region was due to increased nutri- intensity as was reported in regional scale across ent enrichment of coastal waters as well as natural the Gulf and Sea of Oman (Glibert, 2007; meteorological and oceanographic forcings. Thangaraja et al., 2007; Richlen et al., 2010; The fish-killing dinoflagellate C. polykrikoides Sheppard et al., 2010; Al Gheilani et al., 2011; (currently accepted taxonomic synonym is Al-Yamani et al., 2012) and globally (e.g. Margalefidinium polykrikoides) was recently Anderson et al., 2012; Glibert et al., 2018). A detected in Kuwait’s waters in low concentrations wide range of presumed toxic species contribute (Al-Yamani and Saburova, 2019), and hence, the phytoplankton composition of the Gulf and needs monitoring attention, especially following the adjacent waters (Glibert et al., 2002; the previous extensive blooms in the region that Thangaraja et al., 2007; Al-Kandari et al., 2009; affected fisheries, desalination plants, and the Al Gheilani et al., 2011; Al-Yamani et al., 2012; economies of the impacted countries. Al-Yamani and Saburova, 2019). Recently conducted toxin analysis in Qatari waters have revealed a series of phytotoxins including para- Conclusions lytic, diarrhetic and amnesic shellfish toxins, pin- natoxin, cyclic imines and polyether-lactone The Gulf is characterized by having extreme toxins (Al Muftah et al., 2016). Their presence conditions, especially with regard to temperature can be regarded as latent hazards for human and salinity. These conditions coupled with the health in the Gulf region and requires more potential impact of climate change, and the dif- detailed and comprehensive studies through the ferent anthropogenic activities on the marine entire Gulf. environment most probably have impacts on the The most notable bloom of the ichthyotoxic marine biota and the Gulf’s ecosystems. The inci- dinoflagellate Cochlodinium polykrikoides dences discussed above and the marine mortal- affected the Gulf, the Strait of Hormuz, and the ities in Kuwait’s waters that mostly occurred in Sea of Oman in 2008-2009. This was the first highly polluted and eutrophic Sulaibikhat Bay, HAB event associated with C. polykrikoides in signify the urgent need to take action to improve this region. The bloom was outstanding for its the health of the marine environment. Kuwait is geographical coverage, intensity, and unusual keen to fulfill the United Nations Strategic duration from August 2008 through May 2009. It Development Goal (SDG) 13 concerning the inte- caused massive fish kills in Iran, Oman, and gration of climate change measures into national United Arab Emirates (UAE), damaged coral policies, strategies, and planning, as well as SDG reefs, restricted fishing activities, and forced the 14, that deals with conservation and sustainable closure of desalination plants in Oman and UAE use of the seas and marine resources for sustain- (Richlen et al. 2010; Hamzehei et al. 2013). This able development, which includes reducing nutri- was the first HAB event that affected a signifi- ent pollution by 2025, and increase scientific cant part of the Gulf and the adjacent waters, knowledge through research, and by 2020, con- with more than 1,200 km of coastline implicated. serve at least 10 per cent of coastal and marine The progression of the blooms was tracked by areas, consistent with national and international remote sensing by many researchers (e.g. Nezlin law, based on the best available scientific et al., 2010; Polikarpov et al., 2019 and referen- information. ces therein). Monitoring plan to survey Kuwait’s waters for The rRNA gene sequences of C. polykrikoides pollution and algal blooms is initiated. Serious isolated from the Gulf were found to be identical efforts are underway to relocate Sulaibikhat Bay

industrial facilities farther from the coastal area the photographs utilized in this study. The as well as the installation of treatment plants to authors would like to thank the two anonymous reduce discharging of untreated sewage into the reviewers for their helpful comments. We are coastal waters. Moreover, several rehabilitation grateful to Kuwait Institute for Scientific projects are being considered for Kuwait's Research for funding this study under the coastal habitats. FM001O project. In 2017, Kuwait has established a marine protected area (MPA) in Sulaibikhat Bay, which is References undergoing long-term monitoring and management plans. It has an area of approximately Ackleson, S.G., Oitts, D.E., Sullivan, K.D., Reynolds, R.M., 2 1992. Astronaut observations of the Persian (Arabian) 1x2.8 km and activities within the MPA that – impede ecological services are prohibited (e.g. Gulf during STS-45. Geocarto Int. 4, 59 68. doi:10.1080/ 10106049209354389 anchoring, commercial fishing, dumping, and col- Al Gheilani, H.M., Matsuoka, K., Al Kindi, A.Y., Amer, S., lection of marine species). Sulaibikhat Bay was Waring, C., 2011. Fish kill incidents and harmful algal chosen as the MPA site because it has an exten- blooms in Omani waters. J. Agric. Mar. Sci. 16, 23–33. sive productive intertidal zone, is a major nursery doi:10.24200/jams.vol16iss0pp23-33 area of many species of commercial importance, Al-Hashem, M.A., 2017. Gill histopathological effects of and it is highly threatened due to reclamation and PAHs on adult pearl oyster, Pinctada radiata at Al- Khiran coast in Kuwait. J. Environ. Protec. 8, 109–119. urban development pressures, including strong doi:10.4236/jep.2017.82009 sewage and industrial discharges, and hence, offi- Al-Hashem, M.A., Behbehani, M.I., 2016. Polycyclic aro- cial protection of the area would ensure the con- matic hydrocarbons associated with the massive mortal- tinued production of its ecological services. ities of pearl oyster Pinctada radiata at Al-Khiran coast in Important lessons could be learned from other Kuwait during November 2013. In: J.A. Daniels (Ed.), nations that implemented ecosystem approach Advances in Environmental Research, pp. 91–107. Nova restoration, management practices and conserva- Science Publishers, New York. Al-Hassan, R.H., Ali, A.M., Radwan, S.S., 1990. Lipids and tion plans. An example is presented by Hartig their constituent fatty acids of Phaeocystis sp. from the et al. (2019). They suggested that long-term Arabian Gulf. Mar. Biol. 105, 9–14. doi:10.1007/ adaptive management is needed to ensure the sus- BF01344265 tainability of the Gulf’s marine environment, and Al-Kandari, M., Al-Yamani, F., Al-Rifaie, K., 2009. Marine that regional cooperation is needed among Gulf Phytoplankton Atlas of Kuwait’s Waters. Kuwait Institute countries. Regional collaboration in research and for Scientific Research, Kuwait, ISBN 99906-41-24-25. environmental conservation are of high import- Al-Marzouk, A., Duremdez, R., Yuasa, K., Al-Zenki, S., Al- Gharabally, H., Munday B., 2005. Fish kill of mullet Liza ance to all the countries of the Gulf, as they share klunzingeri. In: P. J. Walker, R. G. Lester, M.G. Bondad- the same body of water, and experience similar Reantaso (Eds.), Diseases in Asian aquaculture V: environmental degradation and threats to the Proceedings of the Fifth Symposium on Diseases in Asian Gulf’s marine resources, and they are all devoted Aquaculture, 2002 November 24–28, Queensland, to improving the health of their ecosystems, con- Australia, pp. 143–153. Fish Health Section, Asian serving the marine resources and ensuring the Fisheries Society, Manila. Al Muftah, A., Selwood, A., Foss, A.J., Al-Jabri, H.M.S.J., sustainability of the ecological services. Potts, M., Yilmaz, M., 2016. Algal toxins and producers in the marine waters of Qatar, Arabian Gulf. Toxicon 122, 54–66. doi:10.1016/j.toxicon.2016.09.016 Acknowledgements Al-Muhyi, A.H.A., 2015. The challenges facing Shatt Al Arab River in present and future. Presented at: 7th The authors thank Mr. Walid Al-Zakri and National Conference of the Environment and Natural Mr. Alan Lennox for conducting the sea surveys Resources, 12 November 2015, Basrah, Iraq. and obtaining the oceanographic measurements Al-Mutairi, N., Abahussain, A., El-Battay, A., 2014. Spatial and samples used in this study, Dr. Takahiro and temporal characterizations of water quality in Kuwait – Yamamoto for his assistance with the oxygen Bay. Mar. Pollut. Bull. 83, 127 131. doi:10.1016/j.marpolbul.2014.04.009 profile figures, Dr. Azad Ismail for the histo- Al-Said, T., Naqvi, S.W.A., Ahmed, A., Madhusoodhanan, pathological examination and assessment of fish R., Fernandes, L., Kedila, R., Almansouri, H., Al-Rifaie, specimens, and Dr. Valery Skryabin and Mr. K., Al-Yamani, F., 2019. Heterotrophic consumption may Manickam Nithyanandan for providing some of mask increasing primary production fuelled by

Downloaded from http://read.dukeupress.edu/aehm/article-pdf/23/2/196/899272/196al-yamani.pdf by guest on 29 September 2021 208 Al-Yamani et al. / Aquatic Ecosystem Health and Management 23 (2020) 196–209

anthropogenic nutrient loading in the northern Arabian/ of Kuwait's marine waters: long term impacts of nutrient Persian Gulf. Mar. Pollut. Bull. 148, 30–46. doi:10.1016/j. enrichment. Mar. Pollut. Bull. 100, 607–620. doi:10.1016/ marpolbul.2019.07.054 j.marpolbul.2015.10.022 Al-Yamani, F., Naqvi, S.W.A., 2019. Chemical oceanography Devlin, M.J., Breckels, M., Graves, C.A., Barry, J., Capuzzo, of the Arabian Gulf. Deep-Sea Res. II 161, 72–80. doi:10. E., Huerta, F.P., Al Ajmi, F., Al-Hussain, M.M., 1016/j.dsr2.2018.10.003 LeQuesne, W.J.F., Lyons, B.P., 2019. Seasonal and tem- Al-Yamani, F., Saburova, M., 2019. Harmful algal blooms in poral drivers influencing phytoplankton community in Kuwait’s waters. In: Marine Phytoplankton of Kuwait’s Kuwait marine waters: documenting a changing landscape Waters. Vol. I. Cyanobacteria, Dinoflagellates, in the Gulf. Front. Mar. Sci. 6, 141. doi:10.3389/fmars. Flagellates, pp. 412–431. Kuwait Institute for Scientific 2019.00141 Research, Kuwait, ISBN 978-99966-37-20-9. El-Gindy, A., Hegazi, M., 1996. Atlas on Hydrographic Al-Yamani, F., Al-Ghunaim, A., Subba Rao, D.V., Khan, Conditions in the Arabian Gulf and the Upper Layer of N.Y, Al-Ghool, M., Muruppel, M., Al-Qatma, S., Luis, the Gulf of Oman. University of Qatar, Qatar. M., 2000. Fish Kills, Red Tides, and Kuwait’s Marine Emery, K.O., 1956. Sediments and water of the Persian Gulf. Environment. Kuwait Institute for Scientific Research, AAPG Bull. 40, 2354–2383. Kuwait. Evans, J.J., Klesius, P.H., Glibert, P.M., Shoemaker, C.A., Al-Yamani, F., Ismail, W., Al-Rifaie, K., M’Harzi, A., Rao, Al-Sarawi, M.A., Landsberg, J., Duremdez, R.D., Al D.V.S., Lennox, A., Saeed, T., Al-Ghadban, A.N., Al- Marzouk, A., Al Zenki, S., 2002. Characterization of beta- Matrouk, K., Bahlol, M., Al-Khabaz, M., 2002. hemolytic group B S. agalactiae in cultured sea bream, Oceanographic and environmental assessment of Kuwait Sparus auratus (L.) and wild mullet, Liza klunzingeri Bay in relevance to toxic algal blooms. Kuwait Institute (Day) in Kuwait. J. Fish Dis. 25, 505–513. doi:10.1046/j. for Scientific Research, Final Report FM028K, KISR 1365-2761.2002.00392.x 6558. Glibert, P., 2007. Eutrophication and harmful blooms: a com- Al-Yamani, F.Y., Bishop, J.M., Ramadhan, E., Al-Husaini, plex global issue, examples from the Arabian Sea includ- M., Al-Ghadban, A.N., 2004. Oceanographic Atlas of ing Kuwait Bay, and an introduction to the global ecology Kuwait's Waters. Kuwait Institute for Scientific Research, and oceanography of harmful algal blooms (GEOHAB) Kuwait, ISBN 99906-41-19-6. programme. Int. J. Oceans Oceanogr. 2, 157–169. Al-Yamani, F., Saburova, M., Polikarpov, I., 2012. A prelim- Glibert, P., Landsberg, J., Evans, J., Al-Sarawi, M., Faraj, M., inary assessment of harmful algal blooms in Kuwait’s Al-Jarallah, M., Haywood, A., Ibrahem, S., Klesius, P., marine environment. Aquat. Ecosyst. Health Manag. Powell, C., Shoemaker, C., 2002. A fish kill of massive 15(sup1), 64–72. doi:10.1080/14634988.2012.679450 proportion in Kuwait Bay, Arabian Gulf, 2001: The roles Al-Yamani, F., Yamamoto, T., Al-Said, T., Alghunaim, A., of bacterial disease, harmful algae, and eutrophication. 2017. Dynamic hydrographic variations in Northwestern Harmful Algae 1, 215–231. doi:10.1016/S1568- Arabian Gulf over the past three decades: temporal shifts 9883(02)00013-6 and trends derived from long-term monitoring data. Mar. Glibert, P.M., Berdalet, E., Burford, M.A., Pitcher, G.C., Pollut. Bull. 122, 488–499. doi:10.1016/j.marpolbul.2017. Zhou, M., 2018. Introduction to the Global Ecology and 06.056 Oceanography of Harmful Algal Blooms (GEOHAB) Anderson, D.M., Cembella, A.D., Hallegraeff, G.M., 2012. Synthesis. In: P. Glibert, E. Berdalet, M. Burford, G. Progress in understanding harmful algal blooms: paradigm Pitcher, M. Zhou (Eds.), Global Ecology and shifts and new technologies for research, monitoring, and Oceanography of Harmful Algal Blooms, pp. 3–7. management. Annu. Rev. Mar. Sci. 4, 143–176. doi:10. Ecological Studies (Analysis and Synthesis), 232, 1146/annurev-marine-120308-081121 Springer, Cham. Ben-Hassan, A., Christensen, V., 2019. Vulnerability of the Hamza, W., Munawar, M., 2009. Protecting and managing the marine ecosystem to climate change impacts in the Arabian Gulf: Past, present and future. Aquat. Ecosyst. Arabian Gulf - an urgent need for more research. Glob. Health Manag. 12(4), 429–439. doi:10.1080/ Ecol. Conserv. 17(2), e00556. doi:10.1016/j.gecco.2019. 14634980903361580 e00556 Hamzehei, S., Bidokhti, A.A., Mortazavi, M., Gheiby, A., Burt, J., Van Lavieren, H., Feary, D., 2014. Persian Gulf 2013. Red tide monitoring in the Persian Gulf and Gulf of reefs: an important asset for climate science in urgent Oman using MODIS sensor data. Tech. J. Engin. App. need of protection. Ocean Challenge 20, 49–56. Sci. 3(12), 1100–1107. Cavalcante, G.H., Feary, D.A., Burt, J.A., 2016. The influence Hartig, J.H., Munawar, M., Hamza, W., Al-Yamani, F., 2019. of extreme winds on coastal oceanography and its impli- Transferring lessons learned from use of an ecosystem cations for coral population connectivity in the southern approach to restore degraded areas of North American Arabian Gulf. Mar. Pollut. Bull. 105, 489–497. doi:10. Great Lakes to the Arabian Gulf. Aquat. Ecosys. Health 1016/j.marpolbul.2015.10.031 Manag. 22(2), 149–159. doi:10.1080/14634988.2019. Devlin, M.J., Massoud, M.S., Hamid, S.A., Al-Zaidan, A., 1622986 Al-Sarawi, H., Al-Enezi, M., Al-Ghofran, L., Smith, A.J., Heil, C., Glibert, P., Al-Sarawi, M.A., Faraj, M., Behbehani, Barry, J., Stentiford, G.D., Morris, S., da Silva, E.T., M., Husain, M., 2001. First record of a fish-killing Lyon, B.P., 2015. Changes in the water quality conditions Gymnodinium sp. bloom in Kuwait Bay, Arabian Sea:

Chronology and potential causes. Mar. Ecol. Progr. Ser. Savrda, C.E., Bottjer, D.J., 1987. The exaerobic zone, a new 214, 15–23. doi:10.3354/meps214015 oxygen-deficient marine biofacies. Nature 327, 54–56. Jafar, Q.A., Al-Zinki, S., Al-Mouqati, S., Al-Amad, S., Al- doi:10.1038/327054a0 Marzouk, A., Al-Sharifi, F., 2009. Molecular investigation Sheppard, C.R.C., Al-Husaini, M., Al-Jamali, F., Al-Yamani, of Streptococcus agalactiae isolates from environmental F., Baldwin, R., Bishop, J., Benzoni, F., Dutrieux, E., samples and fish specimens during a massive fish kill in Dulvy, N.K., Subba Rao, D.V., Jones, D.A., Loughland, R., Kuwait Bay. African J. Microbiol. Res. 31, 22–26. Medio, D., Nithyanandan, M., Pilling, G.M., Polikarpov, I., Jones, D.A., Price, A.R.G., Al-Yamani, F., Al-Zaidan, A., Price, A.R.G., Purkis, S., Riegl, B., Saburova, M., Namin, 2002. Coastal and marine ecology. In: N.Y. Khan, M. K.S., Taylor, O., Wilson, S., Zainal, K., 2010. The Gulf: a Munawar, A.R.G. Price (Eds.), The Gulf Ecosystem: young sea in decline. Mar. Pollut. Bull. 60, 13–38. doi:10. Health and Sustainability, pp. 65–104. Backhuys 1016/j.marpolbul.2009.10.017 Publishers, Leiden, the Netherlands. Shoemaker, C.A., Klesius, P.H., Evans, J.J., 2001. Prevalence Kampf, J., Sadrinasab, M., 2006. The circulation of the of Streptococcus iniae in tilapia, hybrid striped bass and – Persian Gulf: a numerical study. Ocean Sci. 2, 27 41. doi: channel catfish from fish farms in the United States. Am. 10.5194/os-2-27-2006 J. Vet. Res. 62, 174–177. doi:10.2460/ajvr.2001.62.174 KUNA (Kuwait News Agency), 2017. EPA carries on with Subba Rao, D.V., Al-Yamani, F., 1998. Phytoplankton ecol- survey of Kuwait Bay, 4 May 2017. Available: https:// ogy in the water between Shatt Al-Arab and the Straits of www.kuna.net.kw/ArticleDetails.aspx?id=2608470&lan- Hurmuz, Arabian Gulf: a review. Plankton Biol. Ecol. 45, guage=en, accessed 12 October 2019. 101–116. Nezlin, N.P., Polikarpov, I.G., Al-Yamani, F.Y., Rao, D., Subba Rao, D.V., Al-Yamani, F., Lennox, A., Pan, Y., Al- Ignatov, A., 2010. Satellite monitoring of climatic factors Said, T.F.O., 1999. Biomass and production characteristics regulating phytoplankton variability in the Arabian of the first red tide noticed in Kuwait Bay, Arabian Gulf. J. (Persian) Gulf. J. Mar. Syst. 82, 47–60. doi:10.1016/j. Plankton Res. 21(4), 805–810. doi:10.1093/plankt/21.4.805 jmarsys.2010.03.003 Subba Rao, D.V., Al-Hassan, J.M., Al-Yamani, F., Al-Rafaie, Perrone, T.J., 1979. Winter shamal in the Persian Gulf.Naval K., Ismail, W., Nageswara Rao, C.V., Al-Hassan, M., Environmental Prediction Research Facility, Monterey, CA. 2003. Elusive red tides in Kuwait coastal waters. Harmful Polikarpov, I., Al-Yamani, F.Y., Saburova, M., 2009. Space- Algae News 24, 10–13. time variability of phytoplankton structure and diversity in Svobodova, Z., Richard, L., Jana, M., Blanka, V., 1993. the north-western part of the Arabian Gulf (Kuwait’s Water quality and fish health. EIFAC Technical paper 54. waters). In: F. Krupp, L.J. Musselman, M.M.A Kotb, Rome, Food and Agriculture Organization of the United I. Weidig (Eds.), Environment, Biodiversity and Nations. Conservation in the Middle East. Proceedings of the First Thangaraja, M., Al-Aisry, A., Al-Kharusi, L., 2007. Harmful Middle Eastern Biodiversity Congress, Aqaba, Jordan, 20-23 algal blooms and their impacts in the middle and outer October 2008. BioRisk 3, 83–96. doi:10.3897/biorisk.3.8 – Polikarpov, I., Saburova, M., Al-Yamani, F., 2016. Diversity ROPME sea area. Int. J. Oceans Oceanogr. 2, 85 98. and distribution of winter phytoplankton in the Arabian Times of Oman, 2019. Massive cleanup as dead fish wash up Gulf and the Sea of Oman. Cont. Shelf Res. 119, 85–99. at Bandar Al Rowdha, October 13, 2019. Available: https:// doi:10.1016/j.csr.2016.03.009 timesofoman.com/article/2059863/Oman/Environment/ Polikarpov, I., Al-Yamani F., Saburova M., 2019. Remote Massive-cleanup-as-dead-fish-wash-up-at-Bandar-Al-Rowdha, sensing of phytoplankton variability in the Arabian/ accessed 22 October 2019. Persian Gulf. In: Barale, V., Gade, M. (Eds.), Remote Vaquer-Sunyer, R.Duarte, C.M., 2008. Thresholds of hypoxia Sensing of the Asian Seas, pp. 485–501. Springer, Cham. for marine biodiversity. Proc. Natl Acad. Sci. USA 105, – Purser, B.H., Seibold, E., 1973. The principal environmental 15452 15457. doi:10.1073/pnas.0803833105 factors influencing Holocene sedimentation and diagensis. Vaughan, G.O., Burt, J.A., 2016. The changing dynamics of In: B.H. Purser (Ed.), The Persian Gulf, Holocene coral reef science in Arabia. Mar. Pollut. Bull. 105, Carbonate Sedimentation and Diagenesis in a Shallow 441–458. doi:10.1016/j.marpolbul.2015.10.052 Epicontinental Sea, pp. 1–9. Springer-Verlag, Berlin. Vaughan, G.O., Al-Mansoori, N., Burt, J.A., 2018. The Reynolds, R.M., 1993. Physical oceanography of the Gulf, Arabian Gulf. In: C. Sheppard (Ed.), World Seas: An Strait of Hormuz, and the Gulf of Oman - results from the Environmental Evaluation, 2nd Ed., Vol. 2: The Indian Mt Mitchell expedition. Mar. Pollut. Bull. 27, 35–59. Ocean to the Pacific, pp. 1–23. Elsevier Science, Richlen, M.L., Morton, S.L., Jamali, E.A., Rajan, A., Amsterdam. Anderson, D.M., 2010. The catastrophic 2008-2009 red Wilber, D., Clarke, D., 2010. Dredging activities and the tide in the Arabian Gulf region, with observations on the potential impacts of sediment resuspension and sedimenta- identification and phylogeny of the fish-killing dinoflagel- tion on oyster reefs, pp. 61-69. In: Proceedings of the late Cochlodinium polykrikoides. Harmful Algae 9, Western Dredging Association Technical Conference. San 163–172. doi:10.1016/j.hal.2009.08.013 Juan, Puerto Rico, USA.

Downloaded from http://read.dukeupress.edu/aehm/article-pdf/23/2/196/899272/196al-yamani.pdf by guest on 29 September 2021