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 designation of a marine protected area in southern Kuwait Bay that would ensure the continued production of ecological services of the protected Bay area.

Introduction

The Arabian Gulf (referred to here as the Gulf), which is also referred to as the Persian Gulf or Inner Sea of the ROPME Sea Area, is an arm of the Indian Ocean. It is a relatively shallow sea with a mean water depth of 35 m, with depths exceeding 100 m occurring only at the Strait of Hormuz. Extensive shallow regions < 20 m deep, are found off the coasts of Kuwait, Bahrain, and the United Arab Emirates. The Gulf covers an area of 239,000 km2, with a total volume of 7000-8400 km3 (Emery, 1956; Purser and Seibold, 1973; El-Gindy and Hegazi, 1996; Kampf and Sadrinasab, 2006). The Gulf is a marginal sea in an arid zone, with a sub-tropical climate, mostly surrounded by deserts. It has an average rainfall of < 5 cm in coastal Arabia (Al-Yamani et al., 2004). The main freshwater inflow is from the Shatt Al-Arab River, which forms at Qurna where the Tigris and Euphrates Rivers join together and is joined downward by the Karun River before it discharges into the northern Gulf (Al-Muhyi, 2015). The mean surface salinity of the Gulf is about 41 psu. High salinities of the Gulf are due to high evaporation rates, which exceed the sum of precipitation with an annual mean of 34 km3 and river discharge with an annual mean of 37 km3 (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). The Gulf is connected to the Sea of Oman and the Arabian Sea through the Strait of Hormuz, where water exchange between the Gulf and the Sea of Oman occurs. More water of about 3365 km3 year−1 flows into the Gulf than exits the Gulf (3110 km3 year−1) through the Strait of Hormuz (Ackleson et al., 1992).

The general circulation of the Gulf is counter-clockwise, and is mainly driven by halocline forces caused by the high evaporation rates (Reynolds, 1993). The northwesterly or “shamal” wind plays an important role in the large-scale circulation of the Gulf (Perrone, 1979), and influence the coastal currents and storm surges, especially, in the southern basin (Cavalcante et al., 2016).

In recent years, the marine environment of the Gulf has been the focus of many studies, dealing with its oceanographic characteristics, ecology, biodiversity, biogeochemical processes, fisheries and the impacts of natural as well as anthropogenic activities on its ecology and productivity (Hamza and Munawar, 2009; Nezlin et al., 2010; Sheppard et al., 2010; Al-Yamani et al., 2012, 2017; Polikarpov et al., 2016; Al-Said et al. 2019; Al-Yamani and Naqvi, 2019; Devlin et al., 2019).

The extreme conditions of the Gulf, especially with regard to temperatures and the impact on the marine fauna, is driving a growing interest in conducting studies with a focus on the potential impact of climate change on the Gulf’s marine environment and its biota (Burt et al., 2014; Vaughan and Burt, 2016; Ben-Hassan and Christensen, 2019).

An up-to-date review of the current status of the Gulf’s marine environment and ecosystems, the threats to these valuable ecosystems, as well as management efforts to rehabilitate and conserve them is provided by Vaughan et al. (2018). They addressed the subject of climate change as well as the different anthropogenic activities (e.g. coastal development, wastewater discharge, desalination plants, shipping traffic, petroleum industry, and overfishing) and their impacts on the Gulf’s marine systems.

This study summarizes a range of incidents of marine biota mortality in the northwestern Gulf since the first fish kill reported in Kuwait’s waters in 1999 to date, and their possible causes.

Marine life mortality incidences in the northwestern Gulf (a case study in Kuwait’s waters)

Kuwait’s waters in the northwestern Gulf are shallow with a maximum depth of about 30 m, well-mixed, and biologically rich. The seawater temperature ranges from 10 °C to 36 °C, and has a mean salinity of 42 psu (Al-Yamani et al., 2004). However, surface salinity varies in Kuwait’s waters due to the seasonal and interannual fluctuations in the discharge volume of Shatt Al-Arab (Al-Yamani et al., 2004; Al-Said et al. 2019), which is attributed to human intervention in riverine flow upstream (Al-Yamani et al., 2017).

Almost all of Kuwait’s coasts have been modified, except part of the northern coast of Kuwait Bay. Legal and illegal structures (>850 structures including boat ramps, small harbors, piers, jetties, retaining walls and wave breakers, among others) exist on Kuwait’s coast (Al-Mutairi et al., 2014; Devlin et al., 2015). Along Kuwait’s shores, hundreds of hectares of land have been reclaimed and dredged; however, even with these modifications, Kuwait’s coastal zone remains a productive component of the marine ecosystem (Al-Yamani et al., 2004; Sheppard et al., 2010). Probably, some of the artificial structures, such as marinas, can play a positive role for marine life by increasing of diversification of underwater coastal landscapes, providing shelters and food for early life stages and hard substrates for sessile marine organisms, including bio-filtrators, such as sponges.

Kuwait has experienced several incidences of marine mortalities (Fig. 1), the causes of which are numerous and sometimes overlapping. Examples of the causes for the localized die-off of fish and invertebrate populations are natural causes such as hypoxia, as well as other causes such as infectious diseases and parasites, eutrophication and reduction in water quality (due to sewage discharges, agricultural runoff, oil or hazardous waste spills), reduced oxygen concentration in the water column and bottom, harmful and toxic algal blooms, dredging affecting bottom biota, as well as sometimes ‘unknown’ causes. The hypoxic event may be brought on by factors such as algal blooms, high temperatures, and thermal pollution.

Fish kills associated with desalination plants due to thermal pollution and high concentration of free chlorine were reported in 1995, 1996, 1997 and 1998 in Kuwait. Fish mortality was also related to oil spill from the tanker in Kuwaiti waters in 1996 (Al-Yamani et al., 2000). Later, several other factors have been reported as reasons for marine mortalities in Kuwait’s waters (Al-Yamani et al., 2012). The assessment of long-term records of marine mortality in Kuwait’s waters is a challenge since, apart from the two well-documented fish kill reports in 1999 and 2001 in peer reviewed literature (Heil et al., 2001; Glibert et al., 2002), published details are very sparse and not sufficiently documented. Unfortunately, most of the marine mortality reports from the region do not include mortality estimates of the affected species nor estimates of economic loss, which are of high importance. Below the reports of notable mortality incidents in Kuwait’s marine environment are listed and supported by available details including photographs, identification of affected species, measurements of concurrent environmental variables and water quality assessments, and mortality magnitudes whenever possible.

1999 fish mortality and first potentially toxic algal bloom incident

The first recognized potentially toxic algal bloom in Kuwait’s waters was caused by the dinoflagellate Karenia selliformis, previously identified as Gymnodinium sp. (Heil et al., 2001). This bloom occurred during September and October 1999 with an extensive and massive mortality (25 to 30 tons of dead fish) of wild largescale mullets Planiliza macrolepis, together with mortality of approximately 80,000 fish of farmed sobaity (seabream Sparidentex hasta) in mariculture floating cages in Kuwait Bay (Heil et al., 2001). The above incident lead to substantial economic losses for Kuwait estimated to be about 7 million U.S. dollars (Al-Yamani et al., 2002). Whether this dinoflagellate species was ichthyotoxic or that the fish died from secondary harmful effects associated with that bloom still remains uncertain, but it was decided that eutrophication of Kuwait Bay caused by elevated nutrients, potentially from aquaculture activities as well as industrial and untreated sewage inputs, could have caused the initiation and maintenance of the Karenia bloom, which lead to fish mortality in Kuwait Bay (Heil et al., 2001).

2001 fish mortality associated with bacterial infection

In August and September 2001, Kuwait Bay experienced a massive kill of wild Klunzinger’s mullet Liza klunzingeri that resulted in over 2,500 tons of dead fish (Glibert et al., 2002). This event was nearly 100-fold larger than the previous major fish kill of 1999 in this region, which was associated with red tide (Heil et al., 2001).

In early August 2001, dead cultured European gilthead seabream Sparus aurata were observed in the aquaculture cages. The numbers of dead fish per cage per day ranged from roughly 100 to over 1000 by the end of the first week of August. Coincident with this fish kill was the observation of a significant bloom of the dinoflagellate Ceratium furca near the cages site. By mid to late August, the dinoflagellate bloom had dissipated, and the sea bream mortalities in the fish cages were reduced. Concurrently, dead wild mullets were observed in Kuwait Bay. As the fish kill progressed over the following days to weeks, dead and dying mullets were continually observed, in addition to other species of dead and dying fish. These other species, however, represented a minor fraction of the total dead fish, less than 5% (Glibert et al. 2002; Al-Marzouk et al., 2005).

The massive fish mortality in August-September 2001 in Kuwait Bay was attributed to bacterial disease outbreak (Streptococcus agalactiae) rather than to the impact of algal toxins, despite the presence of paralytic shellfish poisoning-related dinoflagellates Gymnodinium catenatum and Pyrodinium bahamense as well as non-toxic bloom-forming dinoflagellates C. furca and Gymnodinium impudicum, which were found in the fish kill area (Glibert et al., 2002).

The bacterium S. agalactiae was implicated as the primary cause of the wild fish kill in Kuwait bay in 2001 (Evans et al., 2002). Streptococcosis is a well-known, global distributed disease affecting both cultured and wild fish. Transmission of infection agents is considered to be a complex interaction between the fish, the pathogens, and the marine environment. It is also a function of the vulnerability of the fish to pathogen (Shoemaker et al., 2001). It was reported that dead fish were rapidly scavenged by smaller fish during the observed fish kill (Glibert et al., 2002), but the extent to which bacteria were transmitted by this pathway is not known. Glibert et al. (2002) hypothesized that the development and subsequent collapse of the dinoflagellate C. furca bloom may have led to stressful conditions that resulted in the initial fish kill in the mariculture cages in early August 2001. Because seabreams were possible carriers of the S. agalactiae, their death, their co-habitation with mullet, and the increased vulnerability of mullet to this pathogen, may have led to the spread of this disease (Glibert et al., 2002). Moreover, Jafar et al. (2009) emphasized the possibility of sewage in Kuwait Bay being the source of infection for fish. Majority of the isolates recovered from mullets exhibited random amplification of polymorphic DNA patterns that were highly similar to those obtained from S. agalactiae recovered from sewage water, thereby implying their common origin (Jafar et al., 2009). Glibert et al. (2002) suggested that nutrient enrichment possibly due to sewage input into the coastal waters was an important factor contributing to the 2001 epizootic fish mortality.

2005 Sardinellas mortality in marinas along Kuwait’s coast

In the morning of August 10, 2005, the surface of small semi-enclosed Ras Al-Ardh marina in Salmiya (Fig. 1A) was covered by dead Fringescale Sardinella Sardinella fimbriata. The surface area of water covered by Sardinellas was estimated approximately to be over 0.07 hectares. Due to high water temperature and low tide, it was assumed that fish schools were probably trapped in the marina by predatory fish. During low tide the Sardinellas were asphyxiated because of low dissolved oxygen concentrations in the seawater within the marina. Dissolved oxygen (DO) concentrations were 1.8, 1.7 and 1.0 mg l−1 in surface, middle and bottom water depths. At salinity of 40 psu and water temperature of 30 °C, such DO concentrations equaled oxygen saturation of 29.7, 28.0 and 16.5%, correspondingly. All these values are hypoxic and lethal for most fish (Svobodova et al., 1993).

2011 summer fish mortalities in marinas along Kuwait’s shores

The second series of massive fish kills in Kuwait’s coastal waters occurred in several marinas in Salmiya area and southwards during summer 2011 (Fig. 1 A, C). First reporting of fish kill incident was registered on June 5, 2011 at 16:00 in Ras Al-Ardh marina. Next day, about thousands of dead fish were observed in a nearby Rescue Station marina (Fig. 2A). The kill consisted of mostly small specimens of Fringescale Sardinella S. fimbriata, 10-12 cm long. Less intensive fish kills were observed also during 7-9 June in several other marinas in the Salmiya area.

It was found that the in-situ DO concentrations in Ras Al-Ardh marina measured by a CTD profiler (JFE Advantech Co., Ltd., Japan) were 1.45 ml l−1 (1.93 mg l−1) on 1 m depth and 0.08 ml l−1 (0.11 mg l−1) near bottom, with 35% and 1.80% of saturation, respectively at water temperature range of 29-30 °C and salinity of 43 psu. At the same day, in the nearby Marina Crescent concentration and saturation of oxygen were 4.84 ml l−1 (6.44 mg l−1) with 116.8% saturation at 1 m depth and 2.47 ml l−1 (3.29 mg l−1) with 58.8% saturation at the bottom. Hypoxic concentrations were observed for several days in several marinas along the shores south of Kuwait Bay.

Chlorophyll-a concentrations ranged from 1.09-9.76 μg l−1 and the dominant phytoplankton species in the fish kill area was small-sized chain-forming diatom Chaetoceros pseudocurvisetus (Fig. 3 E, F) with an average concentration of 2.0 ± 0.8 105 cells l−1, which constituted 49.2% of the total phytoplankton abundance. This diatom is a common bloom-forming species which is observed in Kuwait’s waters (Al-Yamani et al., 2012). Fish pathology investigations have revealed no parasites or viruses in dead fish tissues, but some Gram-negative bacteria (Vibrio sp.) were present that normally are expected to occur when the fish is under stress (Dr. Azad Ismail Saheb, Kuwait Institute for Scientific Research (KISR), Kuwait, pers. comm.).

Most fish cannot live below 30% oxygen saturation. A "healthy" aquatic environment seldom experiences less than 80% oxygen saturation. The minimum dissolved oxygen requirements for tropical marine fish is a concentration of 5 mg l−1 (approximately 75% saturation). These values are minimum requirements for healthy growth, tissue repair and reproduction of fish (Svobodova et al. 1993).

Oxygen saturation data on 6-8 June, 2011 for locations such as Ras Al-Ardh marina, and adjacent semi-closed areas indicated hypoxic condition even at a depth of 1 m (surface layer) with the range of saturation level being between 35 and 14.5%, which is a dangerous level for fish life and survival. Near-bottom saturation levels on the same dates and at same locations can be characterized also as hypoxic, with saturation ranging between 8.5% for Ras Al-Ardh and 0.5% for adjacent areas, which are considered lethal levels for most fish and other marine animals. Vertical profile of oxygen saturation levels at the Rescue Dock on 8 June, 2011 confirmed the abrupt decrease of oxygen saturation level at about 4 m of depth (Fig. 2G). Thus, at the marinas, a near-bottom dysaerobic zone was found at the boundary of anoxic and hypoxic zones, where the life of all aerobic marine organisms was under instant danger (Savrda and Bottjer, 1987).

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

The increase of organic carbon content due to the die-off phase of phytoplankton blooms, and water stratification in semi-enclosed marinas along Kuwait’s shore coincided with the observed oxygen depletion, which might have led to local fish kills during June-July 2011. The probable scenario of fish kill included high organic load (from municipal sewage and decaying algal bloom), with lack of wind and limited water mixing coupled with warm summer temperature and moderate humidity, contributed to the low oxygen concentrations in the water column and, particularly the bottom layer in semi-enclosed marinas, and hence resulted in mortality of schooling Sardines. Fish kills in marinas have been reported elsewhere in the Gulf, such as the latest incident in Muscat, Oman in October 2019. Dr. Sergey Dobretsov from Sultan Qaboos University reported that ardines fish had perished because of a lack of oxygen in the water at nighttime. Sardines are schooling fish, active and move in large numbers, and require large amounts of oxygen, which was not available at night time in the shallow marina waters (Times of Oman, 2019). Another reason was proposed by Mr. Ahmed Al Mashani, in the same newspaper report, stating that the kill occurred when large predator fishes chased Sardines, leading them to enter and get trapped into the shallow 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 recorded within the inshore waters of Kuwait Bay in April-May 2017 (Fig. 3A). The extent of the fish kill area in southern Kuwait Bay was from Kuwait Towers to Doha and Eshairij. The Environment Public Authority (EPA) of Kuwait 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 (KUNA, 2017). Two species of Catfish, Netuma thalassina and Policofollis tenuspinus, were involved in the fish kill. The fish were found dead or in morbid condition (Fig. 1 A, B; 3A). In addition, some morbid and dead mullets L. klunzingeri were also reported later in April in Kuwait Bay.

DO concentrations in the coastal waters of Sulaibikhat Bay off Shuwaikh were moderate to high during day-time sampling, with highest concentration of 11.69 mg l−1 recorded on April 12, 2017, and the lowest concentration of 3.28 mg l−1 recorded toward the bottom on April 23. In fact, over two-thirds of the day-time measurements yielded DO exceeding 5 mg l−1. Hence, the oxygen levels were well above the threshold level of hypoxia (2 mg O2 per liter or lower) known to significantly impact marine life (Vaquer-Sunyer and Duarte, 2008). However, hypoxic (DO < 2 mg l−1) and even anoxic (DO < 0.5 mg l−1) conditions were encountered by CTD profiling in the Shuwaikh Port area on April 30, 2017. Hypoxia was found at a depth of 10 m, and anoxic conditions were found at the bottom (10.6 m), while surface DO, were even higher than 9 mg l−1 (Fig. 3B).

Histopathology examination revealed no bacterial pathology but showed the gills to be inflamed (Dr. Azad Ismail Saheb, KISR, Kuwait, pers. comm.). Microscopic investigations of Catfish gills detected hypertrophied lamellar epithelial cells and ballooning of the lamellar epithelium. Enlarged mucus cells, especially, those at the tips of the secondary lamellae and enlargement of the chloride cells indicated stress-mediated response (Fig. 3 H, I). Excess production of mucus which in turn blocks the respiratory surface could result in a state of hypoxia for the fish, not related to the dissolved oxygen levels in seawater at the time of fish mortality.

High biomass phytoplankton blooms associated with Catfish mortality were recorded along the southern shore of Kuwait Bay in Shuwaikh and Sulaibikhat Bay in June 2015, April-May 2017, and May 2019. Although the total phytoplankton abundance varied significantly within the areas associated with fish mortality among the years (1.8 106 – 5.8 108 cells l−1), the observed phytoplankton composition was almost identical with respect to the dominant species. Phytoplankton within the areas associated with fish mortality in 2015, 2017 and 2019 was found to be strongly diatom-dominated. The small-sized chain-forming centric diatoms Thalassiosira spp. and Skeletonema grevillei (Fig. 3 C-G) as well as the tiny pennate diatoms Nitzschia cf. laevis and Nitzschia pusilla dominated the phytoplankton numerically and jointly contributed more than 94-99% of the total phytoplankton abundance. The genus Thalassiosira was manifested in scanning electron microscope as a diverse species complex that included more than ten distinct taxa. Among them, Thalassiosira concaviuscula was found to be the most abundant and bloom-forming species (Fig. 3 C, D).

The phytoplankton blooms were followed by extensive fish mortality in Kuwait Bay that became especially serious in April 2017. The mortality could have occurred due to one or more of the following factors: direct impact of pollution from sewage discharge, or hypoxia caused by decay of organic matter produced by algae and/or sewage together with near-bottom sediment anoxia.

Because mostly Catfish species mortality was reported during this incident, it was presumed that the main reason could be near bottom oxygen depletion, especially during night-time. Toxicity of dissolved ammonia (from discharged sewage) can significantly increase at low oxygen saturation levels (Svobodova et al., 1993), and this factor could also contribute to fish mortality.

2013 massive Mollusks mortality in Khiran

Massive mortality of the pearl oyster Pinctada radiata and scallop Chlamys livida, was recorded in the Khiran area along Kuwait’s southern shore in October and November 2013 (Fig. 1A, E). Numerous valves of the dead Mollusks washed out onto the Khiran shore (Fig. 1E). Along with Mollusks mortality, a few dead Crabs, Sea Cucumbers, and fish were observed in the same area.

Phytoplankton or microphytobenthic blooms were not detected in the Khiran area, suggesting that the observed Mollusk’s mortality event was not linked to a microalgal bloom and the mortality was likely caused by other factors, and most probably by the intensive dredging activities of the nearby mega Khiran residential/chalet project, especially that dredging occurred in the proximity of dense oyster beds in Khiran. Dredging increases suspended sediment loading in the water, causing either the direct burial of oyster beds or reductions in the filtration efficiency and respiration rates of the affected oysters (Wilber and Clarke, 2010). Hence, dredging could have been a factor in the Mollusks’ mortality.

Studies conducted by Al-Hashem and Behbehani (2016) and Al-Hashem (2017) on adult pearl oyster P. radiata collected from the Khiran coast during the November 2013 mass mortality incidence indicated contamination by polycyclic aromatic hydrocarbons (PAHs). The oyster samples displayed histopathological changes in gills as well as necrosis and edemas of branchial lamellae, complete degeneration of gill filaments, loss of regular shape and hemolysis, and inflammation. The study by Al-Hashem and Behbehani (2016) reported the detection of PAHs in sea water, sediment and oyster tissues, and concluded that the PAHs-caused severe histopathological changes in the gills of P. radiata and hence, could be one of the reasons for the oyster mortality at Al-Khiran beach in November 2013.

2018 Sea Cucumber mortality at Kuwait’s southern shore

An incident of Sea Cucumbers mortality was recorded in December 2018 at Kuwait’s southern shore near Mina Al-Shuaiba (Fig. 1A, D). A large number of dead Sea Cucumbers, Holothuria arenicola, were washed ashore at the beach (Fig. 1D), many were dead while others were in a moribund state. The site where the mortality happened is a sandy beach interspersed with fossilized reefs and rocky outcrops near the littoral zone. H. arenicola are mostly seen deeply buried in the sand underneath the rocks and are active deposit feeders. No water discoloration or abnormal water odor were reported at the site. However, storm water discharge of rain water to the beach was noted.

At the beach where dead holothurians were found, both pelagic and benthic microalgae were abundant. However, no potentially harmful microalgal species to marine invertebrates were recorded in the composition of the microalgal assemblages. The abundance of the pelagic microalgal fraction was essentially dominated by nanoflagellates. The small-sized cryptophycean flagellates (aff. Plagioselmis prolonga) were the most abundant and bloom-forming. The sand-dwelling microalgal fraction was predominated by naviculoid diatoms.

The Sea Cucumbers were most likely stressed in situ by an unknown factor, washed up from the bottom sediments, and then the affected Sea Cucumbers died and washed ashore. The most plausible cause is that a sudden decline in salinity from 45 to 5 psu in the nearshore waters occurred due to rainwater discharge from a rain water drain, which likely caused an osmotic shock to the Sea Cucumbers during the ebb tide, and led to their mortality. Many holothurians were observed on the beach in a moribund state.

Harmful Algal Bloom incidences in Kuwait’s waters

Seasonal phytoplankton blooms are part of the annual succession in marine ecosystems and are typical phenomena in Kuwait’s waters as well as in the Gulf region and the adjacent Sea of Oman (e.g. Subba Rao and Al-Yamani, 1998; Jones et al., 2002; Al-Yamani et al., 2004, 2012; Nezlin et al., 2010; Polikarpov et al., 2009, 2016; Sheppard et al., 2010; Al-Yamani and Saburova, 2019). Microalgal blooms occur in Kuwait’s waters year round and are caused by proliferation of diatoms, dinoflagellates, cryptophytes, prymnesiophytes, raphidophytes, chlorophytes, cyanobacteria, and ciliates (Al-Kandari et al., 2009; Al-Yamani et al., 2012, Al-Yamani and Saburova, 2019). The first documented algal blooms in Kuwait’s waters were caused by the colonial prymnesiophyte algae Phaeocystis sp. (Al-Hassan et al., 1990), and the photosynthetic ciliate Myrionecta rubra (Subba Rao and Al-Yamani, 1998). Many other algal bloom events have been documented since then (Subba Rao et al., 1999, 2003; Al-Yamani et al., 2000, 2012; Al-Kandari et al., 2009; Al-Yamani and Saburova, 2019).

Phytoplankton blooms were largely associated with coastal waters along Kuwait’s shore, with Kuwait Bay experiencing most of the harmful algal bloom (HAB) incidents. Diatom-dominated blooms were recorded more frequent than other microalgal groups and were most widely distributed across Kuwait’s waters with high frequency of occurrence in Kuwait Bay. Dinoflagellate-, flagellate- and ciliate-dominated bloom events were mainly restricted to Kuwait Bay and adjacent coastal waters, whereas rare cyanobacterium-dominated blooms were associated with southern Kuwait’s waters exclusively. Species belonging to the genera Chaetoceros, Nitzschia, Thalassiosira and Skeletonema were among the most commonly bloomed diatoms. Karenia papilionacea was the most frequently bloomed dinoflagellate species, and cryptophyceans, raphidophycean Heterosigma akashiwo and colonial haptophyte Phaeocystis globosa were most common bloom-forming flagellates.

Kuwait’s marine environment has been increasingly affected by HABs (Fig. 4). Most of the algal blooms reported so far in Kuwait are harmless to human health, however, such blooms may have deleterious impact including the development of high biomass, leading to oxygen depletion, shading of submerged aquatic plants, alteration of food webs, and suffocation of fish from mucus production and gill interference, leading to fish kills and other environmental and economic outcomes (Subba Rao et al., 1999, 2003; Al-Yamani et al., 2000, 2004, 2012; Glibert, 2007; Al-Yamani and Saburova, 2019).

Harmful Algal Blooms in the Gulf and Sea of Oman

Over the past decades, the occurrence of algal blooms has increased both in frequency and intensity as was reported in regional scale across the Gulf and Sea of Oman (Glibert, 2007; Thangaraja et al., 2007; Richlen et al., 2010; Sheppard et al., 2010; Al Gheilani et al., 2011; Al-Yamani et al., 2012) and globally (e.g. Anderson et al., 2012; Glibert et al., 2018). A wide range of presumed toxic species contribute the phytoplankton composition of the Gulf and the adjacent waters (Glibert et al., 2002; Thangaraja et al., 2007; Al-Kandari et al., 2009; Al Gheilani et al., 2011; Al-Yamani et al., 2012; Al-Yamani and Saburova, 2019). Recently conducted toxin analysis in Qatari waters have revealed a series of phytotoxins including paralytic, diarrhetic and amnesic shellfish toxins, pinnatoxin, cyclic imines and polyether-lactone toxins (Al Muftah et al., 2016). Their presence can be regarded as latent hazards for human health in the Gulf region and requires more detailed and comprehensive studies through the entire Gulf.

The most notable bloom of the ichthyotoxic dinoflagellate Cochlodinium polykrikoides affected the Gulf, the Strait of Hormuz, and the Sea of Oman in 2008-2009. This was the first HAB event associated with C. polykrikoides in this region. The bloom was outstanding for its geographical coverage, intensity, and unusual duration from August 2008 through May 2009. It caused massive fish kills in Iran, Oman, and United Arab Emirates (UAE), damaged coral reefs, restricted fishing activities, and forced the closure of desalination plants in Oman and UAE (Richlen et al. 2010; Hamzehei et al. 2013). This was the first HAB event that affected a significant part of the Gulf and the adjacent waters, with more than 1,200 km of coastline implicated. The progression of the blooms was tracked by remote sensing by many researchers (e.g. Nezlin et al., 2010; Polikarpov et al., 2019 and references therein).

The rRNA gene sequences of C. polykrikoides isolated from the Gulf were found to be identical to isolates from the northeastern USA, Puerto Rico, Mexico, and Malaysia, known as the ‘‘American/Malaysian’’ ribotype (Richlen et al., 2010). Richlen et al. (2010) stated that the occurrence of C. polykrikoides in the Gulf waters was due to the global expansion of this taxon possibly by the introduction of this species through ballast water discharge. Recent increase in HAB impacts observed in this region was due to increased nutrient enrichment of coastal waters as well as natural meteorological and oceanographic forcings.

The fish-killing dinoflagellate C. polykrikoides (currently accepted taxonomic synonym is Margalefidinium polykrikoides) was recently detected in Kuwait’s waters in low concentrations (Al-Yamani and Saburova, 2019), and hence, needs monitoring attention, especially following the previous extensive blooms in the region that affected fisheries, desalination plants, and the economies of the impacted countries.

Conclusions

The Gulf is characterized by having extreme conditions, especially with regard to temperature and salinity. These conditions coupled with the potential impact of climate change, and the different anthropogenic activities on the marine environment most probably have impacts on the marine biota and the Gulf’s ecosystems. The incidences discussed above and the marine mortalities in Kuwait’s waters that mostly occurred in highly polluted and eutrophic Sulaibikhat Bay, signify the urgent need to take action to improve the health of the marine environment. Kuwait is keen to fulfill the United Nations Strategic Development Goal (SDG) 13 concerning the integration of climate change measures into national policies, strategies, and planning, as well as SDG 14, that deals with conservation and sustainable use of the seas and marine resources for sustainable development, which includes reducing nutrient pollution by 2025, and increase scientific knowledge through research, and by 2020, conserve at least 10 per cent of coastal and marine areas, consistent with national and international law, based on the best available scientific information.

Monitoring plan to survey Kuwait’s waters for pollution and algal blooms is initiated. Serious efforts are underway to relocate Sulaibikhat Bay industrial facilities farther from the coastal area as well as the installation of treatment plants to reduce discharging of untreated sewage into the coastal waters. Moreover, several rehabilitation projects are being considered for Kuwait's coastal habitats.

In 2017, Kuwait has established a marine protected area (MPA) in Sulaibikhat Bay, which is undergoing long-term monitoring and management plans. It has an area of approximately 1x2.8 km2 and activities within the MPA that impede ecological services are prohibited (e.g. anchoring, commercial fishing, dumping, and collection of marine species). Sulaibikhat Bay was chosen as the MPA site because it has an extensive productive intertidal zone, is a major nursery area of many species of commercial importance, and it is highly threatened due to reclamation and urban development pressures, including strong sewage and industrial discharges, and hence, official protection of the area would ensure the continued production of its ecological services.

Important lessons could be learned from other nations that implemented ecosystem approach restoration, management practices and conservation plans. An example is presented by Hartig et al. (2019). They suggested that long-term adaptive management is needed to ensure the sustainability of the Gulf’s marine environment, and that regional cooperation is needed among Gulf countries. Regional collaboration in research and environmental conservation are of high importance to all the countries of the Gulf, as they share the same body of water, and experience similar environmental degradation and threats to the Gulf’s marine resources, and they are all devoted to improving the health of their ecosystems, conserving the marine resources and ensuring the sustainability of the ecological services.

Acknowledgements

The authors thank Mr. Walid Al-Zakri and Mr. Alan Lennox for conducting the sea surveys and obtaining the oceanographic measurements and samples used in this study, Dr. Takahiro Yamamoto for his assistance with the oxygen profile figures, Dr. Azad Ismail for the histopathological examination and assessment of fish specimens, and Dr. Valery Skryabin and Mr. Manickam Nithyanandan for providing some of the photographs utilized in this study. The authors would like to thank the two anonymous reviewers for their helpful comments. We are grateful to Kuwait Institute for Scientific Research for funding this study under the FM001O project.

References

Ackleson, S.G., Oitts, D.E., Sullivan, K.D., Reynolds, R.M.,
1992
.
Astronaut observations of the Persian (Arabian) Gulf during STS-45
.
Geocarto Int
.
4
,
59
68
. doi:
Al Gheilani, H.M., Matsuoka, K., Al Kindi, A.Y., Amer, S., Waring, C.,
2011
.
Fish kill incidents and harmful algal blooms in Omani waters
.
J. Agric. Mar. Sci
.
16
,
23
33
. doi:
Al-Hashem, M.A.,
2017
.
Gill histopathological effects of PAHs on adult pearl oyster, Pinctada radiata at Al-Khiran coast in Kuwait
.
J. Environ. Protec
.
8
,
109
119
. doi:
Al-Hashem, M.A., Behbehani, M.I.,
2016
. Polycyclic aromatic hydrocarbons associated with the massive mortalities of pearl oyster Pinctada radiata at Al-Khiran coast in Kuwait during November 2013. In: J.A. Daniels (Ed.),
Advances in Environmental Research
, pp.
91
107
.
Nova Science Publishers
,
New York
.
Al-Hassan, R.H., Ali, A.M., Radwan, S.S.,
1990
.
Lipids and their constituent fatty acids of Phaeocystis sp. from the Arabian Gulf
.
Mar. Biol
.
105
,
9
14
. doi:
Al-Kandari, M., Al-Yamani, F., Al-Rifaie, K.,
2009
.
Marine Phytoplankton Atlas of Kuwait’s Waters
.
Kuwait Institute for Scientific Research
,
Kuwait
, ISBN 99906-41-24-25.
Al-Marzouk, A., Duremdez, R., Yuasa, K., Al-Zenki, S., Al-Gharabally, H., Munday B.,
2005
. Fish kill of mullet Liza klunzingeri. In: P. J. Walker, R. G. Lester, M.G. Bondad-Reantaso (Eds.),
Diseases in Asian aquaculture V: Proceedings of the Fifth Symposium on Diseases in Asian Aquaculture
, 2002 November 24–28, Queensland, Australia, pp.
143
153
. Fish Health Section,
Asian Fisheries Society
,
Manila
.
Al Muftah, A., Selwood, A., Foss, A.J., Al-Jabri, H.M.S.J., Potts, M., Yilmaz, M.,
2016
.
Algal toxins and producers in the marine waters of Qatar, Arabian Gulf
.
Toxicon
122
,
54
66
. doi:
Al-Muhyi, A.H.A.,
2015
.
The challenges facing Shatt Al Arab River in present and future
.
Presented at: 7th National Conference of the Environment and Natural Resources
, 12 November 2015,
Basrah, Iraq
.
Al-Mutairi, N., Abahussain, A., El-Battay, A.,
2014
.
Spatial and temporal characterizations of water quality in Kuwait Bay
.
Mar. Pollut. Bull
.
83
,
127
131
. doi:
Al-Said, T., Naqvi, S.W.A., Ahmed, A., Madhusoodhanan, R., Fernandes, L., Kedila, R., Almansouri, H., Al-Rifaie, K., Al-Yamani, F.,
2019
.
Heterotrophic consumption may mask increasing primary production fuelled by anthropogenic nutrient loading in the northern Arabian/Persian Gulf
.
Mar. Pollut. Bull
.
148
,
30
46
. doi:
Al-Yamani, F., Naqvi, S.W.A.,
2019
.
Chemical oceanography of the Arabian Gulf
.
Deep-Sea Res. II
161
,
72
80
. doi:
Al-Yamani, F., Saburova, M.,
2019
. Harmful algal blooms in Kuwait’s waters. In:
Marine Phytoplankton of Kuwait’s Waters. Vol. I. Cyanobacteria, Dinoflagellates, Flagellates
, pp.
412
431
.
Kuwait Institute for Scientific Research
,
Kuwait
, ISBN 978-99966-37-20-9.
Al-Yamani, F., Al-Ghunaim, A., Subba Rao, D.V., Khan, N.Y, Al-Ghool, M., Muruppel, M., Al-Qatma, S., Luis, M.,
2000
.
Fish Kills, Red Tides, and Kuwait’s Marine Environment
.
Kuwait Institute for Scientific Research
,
Kuwait
.
Al-Yamani, F., Ismail, W., Al-Rifaie, K., M’Harzi, A., Rao, D.V.S., Lennox, A., Saeed, T., Al-Ghadban, A.N., Al-Matrouk, K., Bahlol, M., Al-Khabaz, M.,
2002
.
Oceanographic and environmental assessment of Kuwait Bay in relevance to toxic algal blooms
.
Kuwait Institute for Scientific Research
, Final Report FM028K, KISR 6558.
Al-Yamani, F.Y., Bishop, J.M., Ramadhan, E., Al-Husaini, M., Al-Ghadban, A.N.,
2004
.
Oceanographic Atlas of Kuwait's Waters
.
Kuwait Institute for Scientific Research
,
Kuwait
, ISBN 99906-41-19-6.
Al-Yamani, F., Saburova, M., Polikarpov, I.,
2012
.
A preliminary assessment of harmful algal blooms in Kuwait’s marine environment
.
Aquat. Ecosyst. Health Manag
.
15
(
sup1
),
64
72
. doi:
Al-Yamani, F., Yamamoto, T., Al-Said, T., Alghunaim, A.,
2017
.
Dynamic hydrographic variations in Northwestern Arabian Gulf over the past three decades: temporal shifts and trends derived from long-term monitoring data
.
Mar. Pollut. Bull
.
122
,
488
499
. doi:
Anderson, D.M., Cembella, A.D., Hallegraeff, G.M.,
2012
.
Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management
.
Annu. Rev. Mar. Sci
.
4
,
143
176
. doi:
Ben-Hassan, A., Christensen, V.,
2019
.
Vulnerability of the marine ecosystem to climate change impacts in the Arabian Gulf - an urgent need for more research
.
Glob. Ecol. Conserv
.
17
(
2
),
e00556
. doi:
Burt, J., Van Lavieren, H., Feary, D.,
2014
.
Persian Gulf reefs: an important asset for climate science in urgent need of protection
.
Ocean Challenge
20
,
49
56
.
Cavalcante, G.H., Feary, D.A., Burt, J.A.,
2016
.
The influence of extreme winds on coastal oceanography and its implications for coral population connectivity in the southern Arabian Gulf
.
Mar. Pollut. Bull
.
105
,
489
497
. doi:
Devlin, M.J., Massoud, M.S., Hamid, S.A., Al-Zaidan, A., Al-Sarawi, H., Al-Enezi, M., Al-Ghofran, L., Smith, A.J., Barry, J., Stentiford, G.D., Morris, S., da Silva, E.T., Lyon, B.P.,
2015
.
Changes in the water quality conditions of Kuwait's marine waters: long term impacts of nutrient enrichment
.
Mar. Pollut. Bull
.
100
,
607
620
. doi:
Devlin, M.J., Breckels, M., Graves, C.A., Barry, J., Capuzzo, E., Huerta, F.P., Al Ajmi, F., Al-Hussain, M.M., LeQuesne, W.J.F., Lyons, B.P.,
2019
.
Seasonal and temporal drivers influencing phytoplankton community in Kuwait marine waters: documenting a changing landscape in the Gulf
.
Front. Mar. Sci
.
6
,
141
. doi:
El-Gindy, A., Hegazi, M.,
1996
.
Atlas on Hydrographic Conditions in the Arabian Gulf and the Upper Layer of the Gulf of Oman
.
University of Qatar
,
Qatar
.
Emery, K.O.,
1956
.
Sediments and water of the Persian Gulf
.
AAPG Bull
.
40
,
2354
2383
.
Evans, J.J., Klesius, P.H., Glibert, P.M., Shoemaker, C.A., Al-Sarawi, M.A., Landsberg, J., Duremdez, R.D., Al Marzouk, A., Al Zenki, S.,
2002
.
Characterization of beta-hemolytic group B S. agalactiae in cultured sea bream, Sparus auratus (L.) and wild mullet, Liza klunzingeri (Day) in Kuwait
.
J. Fish Dis
.
25
,
505
513
. doi:
Glibert, P.,
2007
.
Eutrophication and harmful blooms: a complex global issue, examples from the Arabian Sea including Kuwait Bay, and an introduction to the global ecology and oceanography of harmful algal blooms (GEOHAB) programme
.
Int. J. Oceans Oceanogr
.
2
,
157
169
.
Glibert, P., Landsberg, J., Evans, J., Al-Sarawi, M., Faraj, M., Al-Jarallah, M., Haywood, A., Ibrahem, S., Klesius, P., Powell, C., Shoemaker, C.,
2002
.
A fish kill of massive proportion in Kuwait Bay, Arabian Gulf, 2001:
The roles of bacterial disease, harmful algae, and eutrophication. Harmful Algae
1
,
215
231
. doi:
Glibert, P.M., Berdalet, E., Burford, M.A., Pitcher, G.C., Zhou, M.,
2018
. Introduction to the Global Ecology and Oceanography of Harmful Algal Blooms (GEOHAB) Synthesis. In: P. Glibert, E. Berdalet, M. Burford, G. Pitcher, M. Zhou (Eds.),
Global Ecology and Oceanography of Harmful Algal Blooms
, pp.
3
7
. Ecological Studies (Analysis and Synthesis), 232,
Springer
,
Cham
.
Hamza, W., Munawar, M.,
2009
.
Protecting and managing the Arabian Gulf: Past, present and future
.
Aquat. Ecosyst. Health Manag
.
12
(
4
),
429
439
. doi:
Hamzehei, S., Bidokhti, A.A., Mortazavi, M., Gheiby, A.,
2013
.
Red tide monitoring in the Persian Gulf and Gulf of Oman using MODIS sensor data
.
Tech. J. Engin. App. Sci
.
3
(
12
),
1100
1107
.
Hartig, J.H., Munawar, M., Hamza, W., Al-Yamani, F.,
2019
.
Transferring lessons learned from use of an ecosystem approach to restore degraded areas of North American Great Lakes to the Arabian Gulf
.
Aquat. Ecosys. Health Manag
.
22
(
2
),
149
159
. doi:
Heil, C., Glibert, P., Al-Sarawi, M.A., Faraj, M., Behbehani, M., Husain, M.,
2001
.
First record of a fish-killing Gymnodinium sp. bloom in Kuwait Bay, Arabian Sea: Chronology and potential causes
.
Mar. Ecol. Progr. Ser
.
214
,
15
23
. doi:
Jafar, Q.A., Al-Zinki, S., Al-Mouqati, S., Al-Amad, S., Al-Marzouk, A., Al-Sharifi, F.,
2009
.
Molecular investigation of Streptococcus agalactiae isolates from environmental samples and fish specimens during a massive fish kill in Kuwait Bay
.
African J. Microbiol. Res
.
31
,
22
26
.
Jones, D.A., Price, A.R.G., Al-Yamani, F., Al-Zaidan, A.,
2002
. Coastal and marine ecology. In: N.Y. Khan, M. Munawar, A.R.G. Price (Eds.),
The Gulf Ecosystem: Health and Sustainability
, pp.
65
104
.
Backhuys Publishers
,
Leiden, the Netherlands
.
Kampf, J., Sadrinasab, M.,
2006
.
The circulation of the Persian Gulf: a numerical study
.
Ocean Sci
.
2
,
27
41
. doi:
KUNA (Kuwait News Agency)
,
2017
. EPA carries on with survey of Kuwait Bay, 4 May 2017. Available: https://www.kuna.net.kw/ArticleDetails.aspx?id=2608470&language=en, accessed 12 October 2019.
Nezlin, N.P., Polikarpov, I.G., Al-Yamani, F.Y., Rao, D., Ignatov, A.,
2010
.
Satellite monitoring of climatic factors regulating phytoplankton variability in the Arabian (Persian) Gulf
.
J. Mar. Syst
.
82
,
47
60
. doi:
Perrone, T.J.,
1979
.
Winter shamal in the Persian Gulf
.
Naval Environmental Prediction Research Facility
,
Monterey, CA
.
Polikarpov, I., Al-Yamani, F.Y., Saburova, M.,
2009
. Space-time variability of phytoplankton structure and diversity in the north-western part of the Arabian Gulf (Kuwait’s waters). In: F. Krupp, L.J. Musselman, M.M.A Kotb, I. Weidig (Eds.),
Environment, Biodiversity and Conservation in the Middle East
. Proceedings of the First Middle Eastern Biodiversity Congress, Aqaba, Jordan, 20-23 October 2008. BioRisk
3
,
83
96
. doi:
Polikarpov, I., Saburova, M., Al-Yamani, F.,
2016
.
Diversity and distribution of winter phytoplankton in the Arabian Gulf and the Sea of Oman
.
Cont. Shelf Res
.
119
,
85
99
. doi:
Polikarpov, I., Al-Yamani F., Saburova M.,
2019
. Remote sensing of phytoplankton variability in the Arabian/Persian Gulf. In: Barale, V., Gade, M. (Eds.),
Remote Sensing of the Asian Seas
, pp.
485
501
.
Springer
,
Cham
.
Purser, B.H., Seibold, E.,
1973
. The principal environmental factors influencing Holocene sedimentation and diagensis. In: B.H. Purser (Ed.),
The Persian Gulf, Holocene Carbonate Sedimentation and Diagenesis in a Shallow Epicontinental Sea
, pp.
1
9
.
Springer-Verlag
,
Berlin
.
Reynolds, R.M.,
1993
.
Physical oceanography of the Gulf, Strait of Hormuz, and the Gulf of Oman - results from the Mt Mitchell expedition
.
Mar. Pollut. Bull
.
27
,
35
59
.
Richlen, M.L., Morton, S.L., Jamali, E.A., Rajan, A., Anderson, D.M.,
2010
.
The catastrophic 2008-2009 red tide in the Arabian Gulf region, with observations on the identification and phylogeny of the fish-killing dinoflagellate Cochlodinium polykrikoides
.
Harmful Algae
9
,
163
172
. doi:
Savrda, C.E., Bottjer, D.J.,
1987
.
The exaerobic zone, a new oxygen-deficient marine biofacies
.
Nature
327
,
54
56
. doi:
Sheppard, C.R.C., Al-Husaini, M., Al-Jamali, F., Al-Yamani, F., Baldwin, R., Bishop, J., Benzoni, F., Dutrieux, E., Dulvy, N.K., Subba Rao, D.V., Jones, D.A., Loughland, R., Medio, D., Nithyanandan, M., Pilling, G.M., Polikarpov, I., Price, A.R.G., Purkis, S., Riegl, B., Saburova, M., Namin, K.S., Taylor, O., Wilson, S., Zainal, K.,
2010
.
The Gulf: a young sea in decline
.
Mar. Pollut. Bull
.
60
,
13
38
. doi:
Shoemaker, C.A., Klesius, P.H., Evans, J.J.,
2001
.
Prevalence of Streptococcus iniae in tilapia, hybrid striped bass and channel catfish from fish farms in the United States
.
Am. J. Vet. Res
.
62
,
174
177
. doi:
Subba Rao, D.V., Al-Yamani, F.,
1998
.
Phytoplankton ecology in the water between Shatt Al-Arab and the Straits of Hurmuz, Arabian Gulf: a review
.
Plankton Biol. Ecol
.
45
,
101
116
.
Subba Rao, D.V., Al-Yamani, F., Lennox, A., Pan, Y., Al-Said, T.F.O.,
1999
.
Biomass and production characteristics of the first red tide noticed in Kuwait Bay, Arabian Gulf
.
J. Plankton Res
.
21
(
4
),
805
810
. doi:
Subba Rao, D.V., Al-Hassan, J.M., Al-Yamani, F., Al-Rafaie, K., Ismail, W., Nageswara Rao, C.V., Al-Hassan, M.,
2003
.
Elusive red tides in Kuwait coastal waters
.
Harmful Algae News
24
,
10
13
.
Svobodova, Z., Richard, L., Jana, M., Blanka, V.,
1993
. Water quality and fish health. EIFAC Technical paper 54. Rome, Food and Agriculture Organization of the United Nations.
Thangaraja, M., Al-Aisry, A., Al-Kharusi, L.,
2007
.
Harmful algal blooms and their impacts in the middle and outer ROPME sea area
.
Int. J. Oceans Oceanogr
.
2
,
85
98
.
Vaquer-Sunyer, R.; Duarte, C.M.,
2008
.
Thresholds of hypoxia for marine biodiversity
.
Proc. Natl Acad. Sci. USA
105
,
15452
15457
. doi:
Vaughan, G.O., Burt, J.A.,
2016
.
The changing dynamics of coral reef science in Arabia
.
Mar. Pollut. Bull
.
105
,
441
458
. doi:
Vaughan, G.O., Al-Mansoori, N., Burt, J.A.,
2018
. The Arabian Gulf. In: C. Sheppard (Ed.),
World Seas: An Environmental Evaluation
, 2nd Ed., Vol. 2: The Indian Ocean to the Pacific, pp.
1
23
.
Elsevier Science
,
Amsterdam
.
Wilber, D., Clarke, D.,
2010
.
Dredging activities and the potential impacts of sediment resuspension and sedimentation on oyster reefs
, pp. 61-69. In:
Proceedings of the Western Dredging Association Technical Conference
.
San Juan, Puerto Rico, USA
.