Dinoflagellates and Saudi Marine Borders: A Special Consideration for Ballast Water, Invasive Species and BWM Convention

Abstract

Background: The Kingdom of Saudi Arabia is adjacent to two vital marine ecosystems; the semi-enclosed Arabian Gulf and the largely landlocked Red Sea. Dinoflagellates are repeatedly found in these bodies of marine water, which serve as significant routes for cargo ships. Through these ships and ballast water, invasive dinoflagellate species and their cysts are introduced. They compete with indigenous species for nutrients and space, cause massive fish kill-off and disturb the ecological balance and biodiversity. To address these threats, the International Convention for the Control and Management of Ships’ Ballast Water and Sediments (BWM Convention) set forth guidelines intended to curtail the dissemination of such detrimental organisms. The Kingdom of Saudi Arabia was one of the co-signatory countries to this Convention. Methods of detection and monitoring include microscopy, molecular characterization and remote sensing, which are employed for the detection and monitoring of these harmful algae, in order to avert disasters such as fish die-offs. The results of several reports confirmed the presence of number of dinoflagellates in both the Arabian Gulf and the Red Sea, some of which are toxin producers, with certain species being highlighted as invasive species whose presence requires a high level of alert. Discussion: The monitoring, the change in engineering of cargo ships and the introduction of advanced surveillance methods, together with the proper treatments of ballast water, are all important security elements that ensure the safe disposal of ballast water without introducing harmful species.

1. Introduction

1.1. General Characteristics of Dinoflagellates

Dinoflagellates are unicellular eukaryotic protists which are classified under the kingdom Chromista (or Protista) [1,2]. Although predominantly marine (around 90% of species) [1], some also inhabit freshwater or brackish environments [3]. They are classified in both the International Code of Botanical Nomenclature and the International Code of Zoological Nomenclature, as they have mixed algal and zoological characteristics. Indeed, many dinoflagellate species are autotrophs, possessing chloroplasts and performing photosynthesis, and are thereby regarded as algae (referred to as dinophytes), whereas the rest are heterotrophs [4,5,6]. Nonetheless, the most widely used term to describe these protists is Dinoflagellates, and it will be hereafter referred to as such. They are characterized by the presence of two flagella for movement: one oriented transversely and the other longitudinally positioned. The latter is equipped with fine hairs to aid in movement and nutrient uptake. In photosynthetic dinoflagellates, the chloroplast is surrounded by three membranes that are not continuous with the endoplasmic reticulum. Within the chloroplast, thylakoids are typically arranged in stacks of three lamellae. Unlike many other photosynthetic organisms, dinoflagellates lack chlorophyll b; instead, chlorophyll a and chlorophyll c₂ are the primary pigments. The green color of these chlorophylls is generally masked by accessory pigments such as peridinin, β-carotene and various xanthophylls, which collectively give the chloroplast a brownish-golden appearance, which is an important characteristic in the classification of these organisms as golden-brown algae (based on their pigment composition) [4]. In addition, pyrenoids, sometimes stalked or partially penetrated by thylakoids, serve as centers for carbon fixation [5]. The photosynthetic machinery in dinoflagellates has some unique features: some form intracellular symbiosis with diatoms in order to derive energy, while others possess a mature plastid that was acquired either from a secondary endosymbiosis that resulted in the emergence of chlorophyll c and peridinin pigments or from tertiary replacement with a haptophyte-type plastid. Moreover, some dinoflagellates possess transient plastids (kleptoplasts) presumably acquired a cryptophyte or haptophyte [7,8]. Most recently, ref. [7] revealed the presence of PsaT and PsaU, two previously unidentified subunits in photosystem I supercomplex.

1.1.1. Nuclear Organization and Internal Cellular Structures

A striking feature of dinoflagellates is their dinokaryon, a unique interphase nucleus in which the chromosomes are highly condensed. During mitosis, a the nuclear envelope remains intact; instead, bundles of spindle microtubules pass through tunnels lined by nuclear membrane. Complementing this nuclear architecture is a complex network of internal tubes known as the pusule, opening near the flagellar bases. Additionally, many dinoflagellates possess trichocysts—organelles capable of explosive discharge—that eject striated, four-sided threads when stimulated [5,9].

1.1.2. The Cell Envelope and Thecal Plates

Dinoflagellates possess flattened vesicles called cortical alveoli. These alveoli are packed into a layer beneath the cell membrane [10]. This layer is called amphiesma (also called the theca). The amphiesma functions as an outer covering or “cell wall” and is a defining characteristic of dinoflagellates. Flattened vesicles have been associated to a family of proteins, named alveolins, which are common to all alveolates, including dinoflagellates [11]. The dinoflagellates that possess a theca are called “armored”. This is because the theca is a robust outer covering made up of flat, polygonal vesicles. These thecal vesicles contain cellulose plates. They typically form a bipartite structure with an upper (epicone) and lower (hypocone). The arrangement, ornamentation (often with ridges, grooves or spines), and the connections between these plates (via intercalary bands) are key taxonomic features and serve to both protect the cell and accommodate growth [5].

1.2. Taxonomy and Life Cycle

The traditional taxonomy of dinoflagellates is mainly based on their morphology, as observed through microscopic examination [12]. Microscopic examination includes both light microscopy and scanning electron microscopy [13]. The photosynthetic dinoflagellates contain chlorophyll a, perform oxygenic photosynthesis and produce starch as a reserve food material resulting from photosynthesis. Dinoflagellates have an epicone and a hypocone, transversed by a horizontal depression called cingulum, and the depression in the cingulum area in the hypocone is called the sulcus [13]. The ventral side of the organism is denoted by the presence of the sulcus [12].

The shape and extent of the sulcus are considered taxonomic markers, as well as the displacement of the cingulum. These markers have taxonomic value both at the genus and at species levels. In addition, the absence of thecal plates underneath the plasma membrane or their presence and the tabulation pattern are all morphological characters that are taxonomically important [12,13,14].

Those that are naked, or lack thecal plates, are called athecate, whereas those with thecal plates made of cellulose are called thecate. There are two main forms of these organisms, and they are divided into two classes according to the two forms: one with an undivided wall and the other with a divided wall. One of the difficulties in using the morphological approach is that some dinoflagellates such as benthic athecate and thinly thecate species are too delicate to isolate and too difficult to culture, as they feed on living preys, which are mostly not available in laboratory cultures [13]. Nowadays, a polyphasic taxonomic approach is adopted by many dinoflagellate taxonomists, who use a combination of characters for a more accurate taxonomy [15,16,17]. This approach includes the use of morphological characters, ultrastructure characteristics and molecular analyses to construct a robust taxonomy [18]. With regard to life cycle, most dinoflagellates exhibit a haplontic life cycle, with only the zygote being diploid before forming a resting hypnozygote. Dinoflagellates can reproduce both asexually and sexually. Asexual reproduction is by binary fission and occurs during favorable conditions. On the other hand, sexual reproduction can be triggered by unfavorable conditions and results in the formation of a zygote, which may develop into a resting cyst for survival or into a new generation of cells after undergoing meiosis [19]. Those resting stages or cysts can be transported from one place to another in ballast water and can cause harmful algal blooms [20]. When ballast water is disposed of in a new marine body, and in the presence of favorable conditions, dinoflagellate cysts germinate and resume their pelagic life cycle.

1.3. Nutritional Strategies and Mutualistic Relationships

Dinoflagellates have both photosynthetic and non-photosynthetic forms. The latter feed heterotrophically on diatoms and other aquatic organisms [16]. The diverse modes of nutrition of dinoflagellates include predation, saprotrophy, photoautotrophy and parasitism [2]. Some species employ an extensible pseudopod called a peduncle to capture and ingest prey—sometimes even organisms much larger than themselves. In other dinoflagellates, chloroplasts originate from endosymbiotic algae that retain vestiges of their own cell membranes, thylakoid organization, and occasionally a reduced nucleus. This endosymbiotic origin is evident in the retention of distinct pigment profiles and storage products, even though the endosymbiont becomes highly integrated with the host cell [9]. Many members of the dinophyta (about 50%) do not have chloroplasts and are therefore obligately heterotrophic; many of the photosynthetic forms are facultative heterotrophs and are able to feed phagotrophically. They ingest bacteria and small planktonic algae. Indeed, mixotrophy is reported in many photosynthetic dinoflagellates [3,21].

1.4. Toxin Production and Implications

Many dinoflagellates produce toxins that can accumulate in the food web and lead to severe human and animal health issues [22,23]. Dinoflagellates release toxins when their population density becomes extremely high, leading to a population crash and release of toxins from dead cells. They may also release toxins as a defense mechanism to deter predators, or as an intentional part of predation to immobilize prey. Toxin production can be influenced by factors such as nutrient availability, grazing pressure and temperature [24]. The released toxins will result in large-scale fish kills, coral reef damage and other environmental disasters. The types of these toxins and their effects were reviewed by [25,26] and references therein. Genera such as Gymnodinium spp., Alexandrium spp. and Pyrodinium spp. produce toxin that causes PSP (paralytic shellfish poisoning), whose symptoms are tingling and numbness in both oral area and the extremities, lack of movement control, drowsiness and, rarely, respiratory paralysis. In addition, the toxin produced by genus of Gymnodium breve is responsible for NSP (neurotoxic shellfish poisoning), which is characterized by nausea, diarrhea and nervous disorders. The dinoflagellates Dinophysis spp. and Prorocentrum spp. cause diarrhetic shellfish poisoning, leading to symptoms such as vomiting and diarrhea. A toxin produced by Azidinium sp. causes AZP (azaspir acid poisoning), which is characterized by vomiting and diarrhea, as well as some neurological symptoms. This toxin is called Azaspiracids (AZAs), exhibits lipophilic properties and can cause shellfish poisoning in humans [27]. Finally, the species Gambierdiscus toxicus produces a toxin that causes gastrointestinal diseases and adversely affects heart and blood vessels. Genera producing those toxins are reported in the Red Sea and/or the Arabian Gulf [13,23,28,29,30]. However, the causative reason behind the recent spread of alien or invasive species and the monitoring of the extent of their spread are scarcely investigated but are most likely related to nutrient richness, climate change and ballast discharge and biofouling, factors discussed later in the review.

1.5. Dinoflagellates Distribution, Abundance and Formation of Harmful Algal Blooms

The multiple unique structural, morphological and physiological attributes allow them to survive and thrive in different habitats and adapt to different conditions. Indeed, dinoflagellates are widely distributed across different parts of the world, including temperate and tropical waters, but tend to be more predominant in warm waters, especially in the tropics, where they are present throughout the year [31]. In temperate regions, they reach their maximum abundance in late spring and summer both in the sea and in fresh water. A spring bloom of diatoms is often followed by rich growths of dinoflagellates. The greatest diversity and maximum abundance of dinoflagellates are encountered in the neritic (nearshore) zones of the oceans, where nutrients from the land are more abundant and where nutrient enrichment may be brought about by upwelling. More specifically, dinoflagellates tend to form “bloom” when the stratification of the water column occurs following the relaxation of upwelling [32]. The chlorophyll maximum at 75–150 m below the surface in nutrient-poor tropical and subtropical areas represents a concentration of tiny planktonic algae belonging to various groups (predominantly cyanophyta, heterokontophyta and haptophyte). These algae, which inhabit in the lower, dim regions of the euphotic zone (the layer where sufficient light penetrates to allow photosynthesis) are probably able to scavenge nutrients from the cold, dark water beneath the euphotic zone. Some species of dinoflagellates are benthic, living on layers of marine sands. In contrast, other species live endosymbiotically in the tissues of invertebrate animals. They live symbiotically in coral reefs, where the endosymbiotic dinophyte is referred to as zooxanthellae. Interestingly, blooms of certain dinoflagellates can light up the sea at night through bio-luminescence. This emission of light, mostly in response to a mechanical disturbance, is responsible for much of the bioluminescence seen in surface waters at night and is believed to be of adaptive value [33]. With regard to the global distribution of dinoflagellates, ref. [34] investigated dinoflagellate diversity and distribution. They demonstrated that fossil cysts can serve as indicators of ancient coastlines and that marine animals with a benthic, dormant cyst stage are restricted to the continental shelf. Within comparable latitudes, the communities in the northern and southern hemispheres are nearly identical, with a strip of circumtropical species separating them. Tropical and polar waters are home to a few indigenous species. Certain benthic dinoflagellates are only found in tropical regions; they include a unique population, some of which cause poisoning in ciguatera fish. Grazing and chemical consequences can be significant in lakes. Predatory dinoflagellates frequently co-exist alongside diatoms, which they consume as prey [34].

1.6. Dinoflagellates and Climate Change

Climate change has a global impact on all living organisms, including dinoflagellates, especially in tropical marine habitats. Through warming waters and altered water chemistry, the growth, distribution and abundance of dinoflagellates can change, leading, in most cases, to harmful blooms, as in the case of the Gulf of Mexico [35]. Rising water temperatures can affect dinoflagellate growth rates. Harmful dinoflagellate species, such as Karenia brevis, may experience increased growth rates under elevated temperatures and higher CO₂ levels. Climate change can also cause dinoflagellates to shift their geographical ranges, potentially expanding into new areas or contracting in others [35]. Dinoflagellates form the base of the marine food web, and changes in their populations can have cascading effects on other organisms. For example, shifts in diatom and dinoflagellate abundance can affect zooplankton and fish populations, as well as alter the availability of certain nutrients.

For example, studies in the East China Sea have shown that warming and eutrophication (excessive nutrient enrichment) have led to a decrease in the relative biomass of diatoms compared to dinoflagellates, with some evidence suggesting that dinoflagellates may be favored in warmer, nutrient-rich conditions [36]. If ongoing climate change continues, there will be habitat shifts and a massive expansion in the distribution of dinoflagellates. Therefore, continued monitoring of dinoflagellate populations and environmental conditions is crucial to track changes and understand the long-term impacts of climate change. Indeed, climate change is having a demonstrable effect on dinoflagellates, with potential consequences for marine ecosystems and human activities. Understanding these impacts and developing effective strategies to mitigate them is a critical area of research.

1.7. The Dispersal of Dinoflagellates and Their Cysts by Ballast Water and Biofouling

Ballast water is defined as the balance water held in tanks of cargo ships, which provides stability and maneuverability during voyages and can contain a mixture of marine and fresh waters, facilitating the dispersal of non-indigenous invasive species and pathogens globally [37]. An example of catastrophic consequences that result from the lack of monitoring of these harmful algae was the 2008–2009 red tide incident in the Arabian Gulf, which was caused by the dinoflagellate Cochlodinium polykrikoides. This incident resulted in massive fish mortality, coral degradation, a decline in local tourism and the temporary closure of the desalination plants in Oman [38]. This dinoflagellate is native to northeastern USA, Mexico and Malaysia and is called the “American/Malaysian” ribotype [38]. The main reason for its widespread distribution in the Arabian gulf is Ballast water discharge. This is a striking example of how this discharge of a single harmful alga can cause massive economic losses and become difficult to contain once it spreads rapidly, especially if it finds warm waters full of nutrients. As the Arabian Gulf is semi-enclosed, with a very slow rate of water renewal, it provides an excellent habitat for harmful algae to flourish. Such events underscore the importance of managing ballast water discharge, which is a major vector for the spread of harmful algal species. Under the BWM Convention [39], countries are required to implement procedures including regular ballast water sampling, the maintenance of detailed log books, and the use of treatment technologies (e.g., filtration, UV sterilization, ozonation, and chemical treatments) to minimize ecological risks [40,41]. Moreover, ref. [37] reported that ballast water can be a vector for the dispersal of Diniflagellates cysts. Encystment happens during unfavorable conditions, for example, low oxygen concentration, low temperature or light intensity. These conditions may occur in ballast tanks, where the encystment helps cells survive the voyage. Otherwise, cysts can be picked up when initially filling tanks with ballast water. As the expansion of dinoflagellate distribution is highly expected due to the combined effect of ongoing climate change and ballast water, which are the primary vectors for introducing harmful dinoflagellates and their cysts to new ecosystems. These introduced cysts can become invasive and cause significant ecological and socioeconomic harm, including harmful algal blooms [20]. Ref. [42] conducted a pioneering study on dinoflagellate cysts from the Red Sea. With regard to cyst composition, they found a total of 19 types of dinoflagellate cysts across the six sites. Cyst numbers ranged from 3 to 4083 cysts per gram of dry sediment. The highest concentrations of cysts were found in sediments with higher percentages of organic carbon, silt and clay. The assemblages were dominated by cysts of potentially toxic species, including Cochlodinium polykrikos, Prorocentrum minimum, Dinophysis acuminata, Alexandrium catenella and Scrippsiella trochoidea. Most cysts were able to germinate. The study concludes that monitoring surface sediments for these cysts is necessary to provide early warnings for the presence of toxic species. Research has also indicated the presence and germination of dinoflagellate cysts in the surface sediments of the Red Sea, particularly near aquaculture wastewater discharges, due to nutrient load, which must be also controlled.

Another risk factor for the dispersal of toxic algae is the “Biofouling” phenomenon. Toxic algae may not only be found in ballast water, but also on marine vehicles through a process known as “biofouling”, as they can cling onto the hull and nestle in small spaces. This phenomenon leads not only to negative environmental impact, but also to negative economic and health impacts. For example, the introduction of harmful invasive species into local waters have several serious consequences, such as competition with local species for space and food, alterations in the ecosystem, a reduction in local biodiversity and even the extinction of native species (https://www.gisp.org/publications/toolkit/BiofoulingGuidelines.pdf (Last accessed on 1 October 2025).

1.8. The Kingdom of Saudi Arabia and the BWM Convention Concerning Regulations of Ballast Water

The international community paid attention to the risks imposed by this phenomenon, as a ballast water management agreement was concluded in 2004, which was adopted by the International Maritime Organization in order to reduce the ballast water risks. Later, the international agreement Convention for the Control and Management of Ships’ Ballast Water and Sediments (BWM) was signed in 2017 to monitor and manage ships’ ballast water and its sediments (http://www.imo.org/en/About/Conventions/ListOfConventions/Pages/International- (Last accessed on 1 October 2025). The signatory countries to the Convention agreed to monitor the ships’ compliance with the standards and procedures that limit the pollution of the local environment with ballast water and its contents.

The BMW agreement was signed by many nations to curtail the dangers of ballast water and reduce the possibility of the dispersal of invasive dinoflagellate species that can compete for nutrients with indigenous species and cause fish die-offs, as well as an imbalance in local biodiversity. The Kingdom of Saudi Arabia is one of the co-signatory countries to this agreement. The Saudi marine borders are the Red Sea and the Arabian Gulf, both semi-closed water bodies with a very low rate of water renewal and high influx of cargo ships. This is due to the fact that Saudi Arabia is the first exporter of oil worldwide. Recently, there have been some records of dinoflagellate species, most of which are toxin-producing and invasive, that have recently emerged in both the Red Sea [23] and the Arabian Gulf.

Therefore, in this review, a detailed account on the biology of dinoflagellates, methods for monitoring and management, as well as a discussion on control measures, as found in the agreement, are provided, with special reference to the Kingdom of Saudi Arabia.

2. Methods of Monitoring and Management of Dinoflagellates

2.1. Traditional Microscopy

The traditional detection of these algae is by light microscopy and scanning electron microscopy [13]. The morphological attributes such as thecal plate tabulation and sulcus and cingulum characteristics are studies by examination under light microscope and inverted microscope in most cases. To date, this is the most widely used method in most labs due to its practicality over other more resources-demanding techniques such as electron microscopy, molecular techniques and the more recent DNA metabarcoding [23].

2.2. Molecular Detection

2.2.1. Molecular Detection of Some Toxic Dinoflagellates

With regard to some of the dinoflagellate species found in red sea, several records were listed by [13,23]. For the purpose of quick surveillance, molecular methods can be used to monitor the presence of those toxin-producing algae in checking facilities at ports. The molecular method is mainly based on the PCR technique using specific primers for some of the genes responsible for toxin biosynthesis [43]. The sequences of those specific primers are provided below:

Alexandrium spp.

F’-GCAADGAATGTCTTAGCTCAA

R’-GCAMACCTTCAAGMATATCCC

Dinophysis spp.

F’-GCACGCATCCAAYTATCCATAAC

R’-CATACAGACACCAACGCAGG

Ostreopsis spp.

F’-AAAACGATATGAAGAGTGCAGC

R’-CCAGGAGTATGCCTACATTCAA

The PCR protocol includes an initial denaturation (94 °C for 1 min), 35 cycles of denaturation (94 °C for 30 s), annealing (50 °C for 90 s) and extension (72 °C for 1 min), followed by a final extension at 72 °C for 10 min. These assays provide crucial early warnings so that remedial actions—such as ozonation or deoxygenation—can be deployed to inhibit the spread of toxic algae.

With regard to the identification of taxa, specific universal primers for algae that were designed by [44] which target 23S rDNA plastid marker are used. This genetic locus discriminates between different algal groups including dinoflagellates. The steps for revealing the algal identity include the extraction of genomic DNA from the dinoflagellate. This genomic DNA is then employed as a template for PCR using the same PCR conditions specified in [44] and the primer pair p23SrV f1 (5 GGA CAG AAAGAC CCT ATG AA 3) and p23SrV r1 (5 TCA GCCTGT TAT CCC TAG AG 3). The amplicon is sequenced by an automated sequencer. Then, using BLAST nucleotide search (https://blast.ncbi.nlm.nih.gov/Blast.cgi?PROGRAM=blastn&BLAST_SPEC=GeoBlast&PAGE_TYPE=Blast%E2%80%A6) (Last accessed on 1 October 2025), the best matches to the sequences will be collected from GenBank and utilized in the reconstruction. Phylogenetic reconstruction is performed to verify the phylogenetic origin of the taxon. These universal primers worked well on dinoflagellates, with the single exception of one Symbiodinium culture [44].

2.2.2. Molecular Detections of Dinoflagellates Cysts

Perini et al., 2019 [20] used qPCR assays to detect and quantify cysts from toxic dinoflagellates species found in the sediment collected from ports. This was done by species-specific standard curves.

2.2.3. Molecular Detection of Dinoflagellates Using DNA Metbarcoding in Saudi Arabia

A more recent approach in the molecular tests for the detection of toxic dinoflagellates is the DNA metabarcoding according to [23,45]. The barcoding approach is a diagnostic tool for species characterization using a short DNA sequence, especially in environmental samples. Ref. [45] used DNA barcoding of the genetic loci mitochondrial cytochrome c oxidase 1 (cox1) and cytochrome b (cob). They examined several primer pairs and the most effective was used in amplifying a 385 bp cob fragment for dinoflagellates identification. This short DNA is easy to sequence and have good taxon resolution.

2.3. Remote Sensing as a Monitoring and Forecasting Tool for Bloom Formation and Distribution

Remote sensing technology is used to monitor harmful algal blooms over large water areas. By detecting the optical signatures of photosynthetic pigments, satellites can track the spatial and temporal dynamics of these blooms [46]. Moreover, monitoring helps in predicting algal blooms and avoiding ramifications that result from these blooms such as fish -die-off [47,48]. The logic behind remote sensing stems from the fact that algae are photosynthetic organisms which possess several photosynthetic pigments. These pigments are chemical compounds which reflect only certain wavelengths of visible light. Each type of pigment reacts with only a narrow range of the spectrum, and as algae need to capture more of the solar energy, they synthesize several pigments. Through satellite imaging and analysis of optics for certain pigments such as chlorophyll, the detection and identification of dinoflagellates and some other algae can be achieved [46]. Remote sensing is a cost-effective tool that helps present catastrophic events such as die-off and red tide through the in-situ monitoring for detecting and quantifying harmful algae at regional areas [47,48]. However, satellite resolution and accuracy can differ from one satellite to the other. For example, ref. [49] used remote sensing in the Galician Rías area in Spain that witnessed periods of dinoflagellate blooms. Such blooms are a serious threat to aquaculture due to production of biotoxins that can kill aquatic animals. Reddish blooms are associated with the non-toxic species Noctiluca scintillans, with some exceptions such as Alexandrium minutum, which is an active producer of paralytic shellfish toxins. They showed that satellite detection can vary from one satellite station to another as the resolution and sensitivity differ considerably. They also reported that remote sensing alone is not enough to confirm the identity and the toxicity of dinoflagellates. Integration with in situ data that are collected from microscopic or molecular analyses is required to confirm the responsible species for red tide. In addition, some differences between AC processors were detected between satellite stations.

Another remote sensing approach is based on the use of UV reflectance instead of visible light for remote sensing of Dinoflagellates. Ultraviolet reflectance technique has been employed to detect blooms by capitalizing on the unique absorption properties of dinoflagellate-produced compounds. Ref. [50] used ultraviolet data from the single ocean pigment sensor of Japanese GCOM-C satellite. As dinoflagellates exhibit a high concentration of mycosporine-like amino acids and release pigmented soluble organic matter, this resulted in the strong absorption of in the UV region of the spectrum. They demonstrated that a ratio of remote sensing reflectance less than 1 between the UV band at 380 nm and the blue band at 443 nm served as an indicator of dinoflagellate bloom of Lingulodinium polyedra off Southern California. They also observed the change from one bloom causing organism to the other where they detected high chlorophyll a regions where the ratios were greater than 1, indicating the transition from dinoflagellate- to diatom- dominated waters.

2.4. Remote Sensing Application in Saudi Arabia

The remote sensing technique was applied for monitoring algal blooms in area extending between cities of Jeddah and Rabigh on the Red Sea [51]. The collected data included spectral indices of chlorophyll a and its concentration; sea surface temperature; the Normalized Difference Turbidity Index; the Surface Scum Index and the Surface Algal Bloom Index; the Normalized Difference Vegetation Index; and the Normalized Difference Water Index. Algal blooms were found to occur more frequently in winter. Those blooms were inversely correlated with temperature and specific humidity, and directly correlated with wind speed. Valley estuaries, were the most suitable area for growth of algae.

3. Results of Previous Studies Regarding Some Dinoflagellates in Saudi Arabian Marine Borders Including Some Invasive Species

There is an obvious scarcity when it comes to studying dinoflagellates in Saudi Arabian Marine Borders. Nonetheless, the available studies have documented the presence of some dinoflagellate genera along Saudi coastal waters in the Arabian Gulf and the Red Sea.

• a—The Red Sea research

The growth of phytoplankton in the northern Red Sea’s (NRS) euphotic layer is solely dependent on the vertical mixing produced by winter Surface waters are highly-saline water due to high evaporation and winter cooling which, in conjunction with surface circulation and wind patterns, nutrient recycling within the system as well as the entry of intermediate water from the nutrient-rich Gulf of Aden [52].

This caused the Red Sea to become highly oligotrophic due to its low precipitation and lack of major river discharge, which sets it apart from other marine ecosystems.

A comprehensive study of the central Red Sea documented high species diversity, identifying 106 species of free-living dinoflagellates in the coastal areas near Saudi Arabia [23]. The same study reported the presence of species that have the potential to cause harmful algal blooms globally. Moreover, research has shown a correlation between aquaculture activity in the Al-Lith region and the prevalence of HABs, suggesting that nutrient discharge from facilities may be a significant factor in the proliferation of dinoflagellates in the area. Another study has documented the broader phytoplankton community along the northern Red Sea coast, identifying a total of 283 species (129 diatoms, 152 dinoflagellates, and 2 cyanophytes) [53].

• b—The Arabian Gulf research

On the other hand, and with regard to Arabian Gulf and Phytoplankton and water quality: A strong, interdependent relationship was found between phytoplankton abundance and water quality, with changes in one affecting the other [29]. This research also identified the dominant phytoplankton species in the region, including dinoflagellates such as Ceratium fusus and Heterosigma sp.

Some of these taxa are of particular importance as they are considered invasive species. The author has examined those taxa before in 2014 in water sample from marine Banat Lake in Germany adjacent to the North Sea (Figure 1). The presence of some of these in cold waters is has been reported before but their presence in tropical semi-closed marine waters such as the Red Sea and the Arabian Gulf is shockingly alarming and imposes questions as to how they were introduced to these remote, semi-closed water bodies and how some of them were rapidly spreading and adapting to the different climate conditions. Indeed, ref. [23] identified a number of dinoflagellates taxa from Red Sea, many of which were first reported. The most plausible explanation of these results is that ballast water and cargo ships played a vital role in introducing some of these invasive species to the local waters. The taxa concerned are found below, and an illustrative map of the distribution of these taxa is provided in the Supplementary Materials, Figure S1.

1. Akashiwa sp.

A non-armored genus implicated in red tide events, as observed in the southeastern Arabian Sea [54].

2. Ceratium sp.

An armored genus with horn-like projections observed in the Arabian Gulfby [28].

3. Dinophysis sp.

A genus that is known for producing a range of toxins—including okadaic acid. These species are recognized by their unique collar-like structures [23] and were found in the Red Sea.

4. Scripseilla sp.

A globally distributed, armored dinoflagellate reported in both the Arabian Gulf and the Red Sea [28,55,56,57].

5. Gymnodinium sp.

A cosmopolitan, unarmored species recorded in Saudi coastal waters [23,42].

6. Azadinium sp.

A genus that is typically associated with cooler marine habitats. This armored species has recently been noted in waters feeding into the Arabian Gulf [58].

7. Protoperidinium sp.

An armored, heterotrophic dinoflagellate that often follows diatom blooms and is a producer of neurotoxins such as azaspiracids [28,42].

8. Heterocapsa sp.

Considered an alien invader in the Arabian Gulf, this thecate species is linked to severe red tide events and high eutrophication levels [59].

9. Procentrum sp.

A toxin-producing dinoflagellate with a distinct, laterally compressed (heart- shaped) morphology.

10. Gyrodinium sp.

A widely distributed, unarmored and heterotrophic species known for its involvement in red tide phenomena [23,28,59].

3.1. Factors That Were Found to Contribute to the Prevalence of Concerning Dinoflagellates

Recent observations in marine environments frequented by cargo vessels have consistently identified some dinoflagellate genera that are of concern. Many of these protists produce toxins, and while some—such as Gyrodinium and Ceratium—are cosmopolitan (thriving in freshwater, brackish and marine settings), others, including Heterocapsa appear to be non-native. For example, ref. [59] isolated Heterocapsa circularisquama from the Arabian Gulf; this species, typically endemic to the Asia-Pacific, has been linked to significant shellfish mortality and heavy losses in bivalve aquaculture. During red tide events, bloom concentrations reached approximately 10⁸ cells·L⁻¹, with this species accounting for 72–83% of the total phytoplankton population. Concurrently, native diatoms such as Thalassiosira delicatula, T. exigua and Minutocellus polymorphus were also abundant. Detailed microscopic examinations, including both light and electron microscopy, of field specimens and lab-cultured isolates have elucidated these morphological characteristics. The dual threat of toxin production and bloom formation by these harmful algae leads to massive die-offs, disrupts native ecosystems by outcompeting indigenous species, and can adversely affect critical infrastructure such as desalination plants in the Red Sea and Arabian Gulf. Limited recent studies on dinoflagellate diversity along Saudi Arabia’s coastlines exacerbate concerns, especially given the slow water renewal in the semi-enclosed Arabian Gulf, which favors the proliferation of harmful species. Factors contributing to the prevalence of concerning dinoflagellates include elevated water temperatures, changes in salinity and nutrient pollution such as increased nitrogen and phosphorus (eutrophication). In addition, the presence of their living preys, such as diatoms, and the viability of the cysts are among the biotic factors affecting their prevalence [60].

3.2. Engineering and Regulatory Considerations for Ballast Water Management

In response to the risks associated with transporting invasive and harmful dinoflagellates via ballast water, several engineering and regulatory measures have been proposed:

1. Ballast water exchange (D1 standard):

Existing vessels are required to perform ballast water exchange in the open ocean—at least 200 nautical miles from land and in waters deeper than 200 m—so that most viable harmful organisms are flushed out before the vessel reaches coastal zones.

2. Ballast water treatment (D2 standard):

Ships built after 8 September 2017, must incorporate onboard ballast management systems, and all vessels are mandated to comply with the D2 standard by 2024. Saudi Arabian ports, which accommodate a high volume of petroleum shipments, now require vessels to submit ballast water reports and samples. These samples are evaluated using bioluminescence-based assays, where light intensity serves as an indirect measure of ATP levels and, by extension, the number of living organisms.

According to the International Maritime Organization (IMO), the D1 requirement necessitates a 95% volumetric exchange using some approved methods, e.g., sequential or flow-through techniques—conducted at a minimum distance of 200 m from the coast and at depths of at least 200 m [61,62]. While this exchange can be challenging under adverse weather conditions, the D2 standard stipulates that ballast water must be treated before discharge. Post-treatment, water should contain fewer than 10 viable organisms per cubic meter (for organisms ≥ 50 μm) and fewer than 10 viable organisms per milliliter (for organisms < 50 μm), with additional constraints on indicator microbes. Approved treatment methods include UV irradiation and ozonation [61]. Moreover, vessels are required to maintain a Ballast Water Record Book documenting water uptake and treatment operations [62].

Additional safety considerations [62,63] include the following:

• Internal loads: the emptying of ballast tanks can induce free surface effects and elevate the vessel’s vertical center of gravity, so dynamic loads must be managed.
• Vessel operations: ensuring an unobstructed sea view (minimum of two ship lengths or 500 m) is vital for navigation safety.
• Pump and piping integrity: frequent use of the ballast system can lead to wear on components, necessitating regular maintenance to avoid over-pumping through air pipes.

3.3. Exemptions from BWM

Under certain conditions, exemptions from ballast water management requirements are permitted. Ref. [64] summarized the exemptions of the BWM Convention under specific circumstances. Ships may be exempted from ballast water management if the ballasting operations are conducted within same location (Regulation A-3.5 of the BWM Convention). The exemption is based on the existence of two risk assessment methods: the first is the Joint Harmonized Procedure [JHP], which compares salinity and target species between donor and recipient harbors, and the second is the Same Risk Area [SRA], which is a biophysical model to determine whether harmful species could naturally spread between ports without regardless of transportation via ballast water (Regulation A-4 of the BWM Convention). However, these exemptions should not be alternatives to ballast water management. Ref. [64] explained that if all ballasting occurs at the same location (Regulation A-3.5 of the BWM Convention), or when risk assessments using methods such as the Joint Harmonized Procedure (JHP) or the Same Risk Area (SRA) indicate minimal transfer risk (Regulation A-4), vessels may be granted exemptions. However, these exceptions are not substitutes for proper management.

4. Discussion

Saudi Arabia is one of the largest oil-exporting countries and thus its marine borders, both the Arabian Gulf and the Red Sea, must be secured from any risks or hazards. However, a large percent of the Arabian Gulf water has been polluted by oil tankers, and many beaches have become threatened with the extinction of marine life. One example is the deterioration of coral reefs as a direct result of the emptying of ballast waters, thereby introducing alien species that destroy original habitats and cause massive aquatic animal die-off [41] and (https://www.climate.gov/news-features/feed/study-links-spread-deadly-coral-disease-ship-ballast-water#:~:text=According%20to%20lead%20author%20Micheal%20Studivan%2C%20an,port%20and%20release%20it%20at%20another%20port; https://persga.org/programmes/reduction-of-navigation-risk-and-marine-pollution: /(Last accessed on 1 October 2025)). This undoubtedly represents an environmental threat not only on the local level but also on the international level for all countries facing a similar danger, as cargo ships move through the marine waters of many countries. Many cases are reported regarding the introduction of non-indigenous dinoflagellate species into new territories through ballast water [65,66,67,68,69] both in the western world and in the Middle East [38]. The latter report showed a case of massive harmful dinoflagellate blooms, with catastrophic economic losses. Complex biotic and abiotic factors control the development of harmful algal blooms, including temperature, nutrient richness and prey availability [60]. Since both the Red Sea and the Arabian Gulf are semi-closed water bodies with low water renewal rate and serve as routes for cargo ships coming to the Kingdom with their ballast water, nutrient enrichment, together with the warm temperatures, creates perfect conditions for the proliferation of dinoflagellates. This, in turn, poses a threat to marine life, food supply and public health, as many dinoflagellates are toxin-producers, can accumulate in marine animals and can cause many toxin-based diseases in humans who eat fish and other animals.

Research on Saudi Arabian dinoflagellates in the past few years has focused on cataloging the species in the Red Sea, with studies identifying high species diversity (over 100 species) and potentially harmful species, as well as investigating the link between nutrient loading from aquaculture and harmful algal blooms (HABs). Ref. [53] studied the diversity and distribution of phytoplankton from the Red Sea and found that Gonyaulacales were the largest order, followed by Dinophysiales and Peridiniales and the genus Tripos (Ceratium), dominated by the presence of 28 species, followed by Protoperidinium. While considering their distribution, most species of Tripo sp. (Ceratium sp.) were ubiquitous in the region. The Duba region recorded the presence of dinoflagellates (Phalacroma rotundatum and Prorocentrum lima), with very low densities. Other work has examined the relationships between water quality and phytoplankton communities, as well as the ecological impact of desalination plants [70,71]. The Arabian Gulf coast is home to numerous desalination plants, and the ecological impact of desalination operations on local plankton communities has been studied. Discharges from desalination plants, containing high salinity and temperature, can alter the local marine environment. The study found that increased temperature can accelerate phytoplankton proliferation, while higher total suspended solids and salinity have other impacts on the ecosystem [70]. In addition, ref. [71] reported that desalination plants are responsible for pollutants added to the Gulf water through outfall systems. Consequently, desalination projects that provide drinking and municipal water must undergo an environmental impact assessment. Harmful algal blooms can form a biofilm on membranes in desalination plants. Therefore, overcoming this problem requires thorough planning and the establishment of desalination plants away from residential areas, polluted niches (whether with ballast water discharge or other pollution sources) and locations with high nutrient load, such as wastewater facilities. This is another reason why these organisms must be monitored and managed, and factors leading to their proliferation must be controlled.

Therefore, the Kingdom of Saudi Arabia was one of the signatory countries to the Convention, aiming to protect its marine borders. Compliance with the Convention and the guidelines for Article 4 includes having unified operational instructions, planning and management, such as the presence of a ballast water log book that shows the dates of filling and emptying each site tank and replenishing water with new sea water. Treatment includes mechanical methods such as filtration and separation and physical methods such as sterilization by ultraviolet rays, ozone, heat or current. Other treatments include ultrasound and using pesticides for living organisms [40]. The treatment method may actually be a combination of these methods. The ships will discharge the ballast at the shore reception facilities approved in the ports. Extensive ports shall require multiple shore-reception facilities. Article 5 requires that when cleaning or repairing ballast tanks, the ship systems of the signatory countries be compatible with the procedures followed for dealing with ballast water. The agreement will only allow the minimum number of living organisms to be present in the ballast water before discharging that water. To ensure that, the ballast water must be treated with approved systems to limit the spread of harmful aquatic organisms. Samples of ballast water must be taken for examination to ensure that it is subject to treatment and that the percentage of life within it is at its lowest level. Agreement with the Convention’s articles emphasizes the safe disposal of ballast water after treatments but this also needs enforcement and close monitoring from the authorities to ensure strict adherence to the convention. From a surveillance point of view, there must be an array of monitoring strategies that include examining samples from ballast water under microscope as well as detection of harmful dinoflagellates by molecular methods. Remote sensing of dinoflagellates is also useful for monitoring vast areas of the marine bodies in order to prevent violation of the convention.

Treatment recommendations for ballast water and bioresources management include ozonation and deoxygenation. In that regard, ref. [72] recommended an ozone dose of 5–11 mg/L for 6 h to inactivate the cysts of dinoflagellate Amphidinium sp. Ozone is applied during ballast intake or shortly afterward. On the other hand, deoxygenation for ship ballast water treatment in very cold water conditions was recommended by [73]. Deoxygenation is the most promising onboard treatment technology to treat ships’ ballast water in order to reduce the risk of species transfer by inducing hypoxia. For ballast water treatment, ref. [72] has recommended an ozone dose of 5–11 mg/L applied over 6 h to inactivate the cysts of dinoflagellates such as Amphidinium sp. In very cold water conditions, deoxygenation (or hydrodeoxygenation) has been proposed as an effective treatment to induce hypoxia and thereby reduce the viability of transported organisms [73].

5. Conclusions and Recommendations

The review deals with an environmental hazard that is often overlooked but largely destructive to marine habitats which is the danger of toxic dinoflagellates and their cysts in ballast water discharge and on the vehicles of aquatic vessels as biofouling algae.

There is a severe lack of information on this subject and the current maritime regulations regarding this point. This, in turn, served as the motivation for writing this review. To the best of our knowledge, this is the first review to examine biological, legal and engineering aspects of the topic in order to provide a holistic understanding of the dangers posed by dinoflagellates contained in ballast water. In addition, the review highlights the presence of some invasive species, different traditional and advanced monitoring techniques, as well as the regulations mentioned in the convention. This study emphasizes the critical need for a comprehensive monitoring and management policy of ballast water to prevent the transfer of toxin-producing dinoflagellates. For more effective environmental protection and to safeguard water supplies, several recommendations are presented here:

1. Training programs should be conducted for biological examiners to accurately identify harmful algal species.

2. Strict monitoring of ballast water records, including source and renewal dates, must be enforced.

3. The treatment methods need to be regularly verified and standardized based on acceptable biological thresholds.

4. Periodic assessments of water sources must be carried out to detect harmful organisms.

5. Modern detection techniques, including DNA-based molecular methods, must be widely adopted.