Environmental Pollutants in the Mediterranean Sea: Recent Trends and Remediation Approaches
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About this ebook
Pollution of the aquatic environment is a real threat across the globe. It is becoming a topic of intense study for researchers. It has been updated and almost completely revised. The Mediterranean Sea has been recognized as a target hotspot of the world as the pollutant concentration in this region is greater than the levels in other oceans.
The book summarizes research on marine pollutants in the Mediterranean Sea. It presents 5 concise reviews focusing on microplastics, rare earth elements and biotoxins – which are now commonly found in the region. The Editors also emphasize on pollution problems in the Mediterranean region, with 2 chapters presenting studies on Lebanon and Morocco, respectively. The book adds to the collective information on Mediterranean marine pollution. Additionally, references are included at the end of each chapter for the benefit of advanced readers.
The contributions also include discussions on important techniques used to monitor and control marine pollution, such as the bio-monitoring of effluents, and ecological impact assessment of microplastic pollution on fish and the environment.
Audience
Students and researchers in environmental science programs; policymakers in Mediterranean environmental agencies.
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Environmental Pollutants in the Mediterranean Sea - Tamer El-Sayed Ali
Biotoxins in the Mediterranean Sea: Lebanon as a Case Study
Abed El Rahman Hassoun¹, ³, *, Ivana Ujević², Milad Fakhri¹, Romana Roje-Busatto², *, Céline Mahfouz¹, Sharif Jemaa¹, Nikša Nazlić²
¹ National Council for Scientific Research, National Center for Marine Sciences, Batroun, Lebanon
² Laboratory of Plankton and Shellfish Toxicity, Institute of Oceanography and Fisheries, Šetalište Ivana Meštrovića 63, Split, Croatia
³ GEOMAR Helmholtz Centre for Ocean Research Kiel, Marine Biogeochemistry, Kiel, Germany
Abstract
Marine biotoxins are naturally occurring chemicals produced by toxic algae. They can be found in seawater and can accumulate in various marine organisms, such as commercial seafood. When contaminated seafood is consumed, these biotoxins can cause poisoning in humans, with varying health consequences depending on the type and amount of toxins. The proliferation of biotoxin-producing algae in the marine environment has dire socio-economic and environmental consequences due to the contamination of water and seafood. Due to the number of factors related to human pressures and climate change impacts, the frequency of marine biotoxins’ occurrence is increasing significantly globally, and in regional seas such as the Mediterranean Sea. In this chapter, we highlight Lebanon in the Eastern Mediterranean Sea, where marine biotoxins were recently studied. The results show for the first time the presence of lipophilic toxins and cyclic imines in marine biota, with values for okadaic acid, dinophysistoxin 1 and 2, pectenotoxin 1 and 2, yessotoxins and azaspiracids below the detection limit (LOD). Levels above LOD were detected for domoic acid (DA), gymnodimine (GYMb), and spirolides (SPXs) in some species/areas. Maximum levels of DA, GYM, and SPXs (3.88 mg DA kg-1, 102.9 µg GYM kg-1, 15.07 µg SPX kg-1) were found in the spiny oyster (Spondylus spinosus) in agreement with the occurrence of Pseudo-nitzchia spp, Gymndinium spp, and Alexandrium spp. DA was below the EU limit but above the lowest observed adverse effect level (0.9 μg g-1) for neurotoxicity in humans and below the acute reference dose (30 µg kg-1 body weight), both established by EFSA. Considering the lowest lethal dose (LD50) after administration of GYM and SPXs to mice, it is unlikely that there is a health risk due to exposure to these toxins from seafood consumption in Lebanon. Nevertheless, the chronic toxicity of DA, GYMs, and SPXs remains unclear, and the effects of repeated
consumption of contaminated seafood need to be investigated. Because biotoxins have been detected in bivalves and commercial species, as well as other organisms in the marine trophic chain, it is evident that species other than bivalves should be monitored, and the spiny oyster (S. spinosus) may play the role of a sentinel species in biotoxin studies. A regular monitoring program is needed to provide reliable, accurate estimates of bloom toxicity and to investigate their potential impact on marine species and human health in Lebanon.
Keywords: Cyclic imines, Emergent pollutants, Lipophilic toxins, Lebanon, Mediterranean sea, Marine biotoxins, Marine biota, Public health, Seafood.
* Corresponding authors Abed El Rahman Hassoun and Romana Roje-Busatto: National Council for Scientific Research, National Center for Marine Sciences, Batroun, Lebanon and Laboratory of Plankton and Shellfish Toxicity, Institute of Oceanography and Fisheries, Šetalište Ivana Meštrovića 63, Split, Croatia; E-mails: abedhassoun@cnrs.edu.lb and rroje@izor.hr
INTRODUCTION
Phytoplankton blooms have been known since the earliest human records (Boni, 1992; Zheng and Klemas, 2018). The global increase in these events has been notable since the 1980s (Smayda, 1990; Boni 1992, Vlamis and Katikou, 2015; Vilariño et al., 2018) and has been attributed to favorable external conditions such as nitrogen/phosphorus resources, pH, and temperature (Stauffer et al., 2020; Zhang et al., 2020). More recently, these blooms have been attributed in part to the effects of ocean warming, marine heat waves, oxygen depletion, eutrophication, and pollution (Gobler et al., 2017; Gobler et al., 2021).
Of more than 70,000 phytoplankton species worldwide (Guiry, 2012), about 300 species can cause red tides
(Hallegraeff et al., 1995; Lindahl, 1998), and of these, more than 100 are producers of natural toxins that generate toxic episodes, known as Harmful Algal Blooms (HABs), that can be dangerous to humans and other organisms (Berdalet et al., 2016).
According to Karlson et al. (2021), HABs can be divided into six main categories based on their adverse effects on the environment and/or human health: 1. Those that produce phytotoxins that accumulate in suspension feeders (bivalves); 2. Those that cause damage to respiratory mechanisms (fish gills) and/or feeding responses through toxin transfer, leading to mortality of fish and other marine life; 3. Blooms with high biomass that cause nuisance effects and/or lead to oxygen depletion; 4. Blooms disrupt the ecosystem and have multiple cascading effects on species interactions; 5. Those that produce aerosolized toxins that affect human respiratory health; and 6. Localized blooms of harmful benthic or epiphytic microalgae differ from planktonic HABs in habitat, mechanisms, and magnitude of adverse effects.
Phytoplankton cells form the base of the marine food chain and are an important food for filter-feeding bivalves and larval fish and crustaceans (Powell et al., 1995; Cloern and Dufford, 2005). Consequently, HABs’ toxins can be bio-accumulated and biomagnified in the marine trophic chain (Orellana et al., 2017), and may be detrimental to plants, animals, people, and ecosystems (Harrness, 2005; Costa et al., 2017). Thus, HABs can generate several socio-economic implications (Visciano et al., 2016; Nwankwegu et al., 2019; Zhongming et al., 2021; Corriere et al., 2021) which often depend on the size, severity, timing, and duration of the event (Qiao and Saha, 2021).
Biotoxins can be divided into hydrophilic and lipophilic molecules that can cause different symptoms: water-soluble toxins that cause Paralytic (PSP) and Amnesic Shellfish Poisoning (ASP), while liposoluble toxins cause Diarrhetic (DSP) and Neurotoxic Shellfish Poisoning (NSP) (FAO/IOC/WHO, 2004; Visciano et al., 2016). Skin contact with contaminated water, inhalation of aerosolized biotoxins, or direct consumption of contaminated seafood can result in the effects of HABs on human health (Visciano et al., 2016; Sonaka et al., 2018).
Lipophilic Toxins (LTs)
Based on their polarity, marine biotoxins can be classified as hydrophilic, lipophilic (LTs), or amphiphilic (Alarcon et al., 2018).
LTs are toxic metabolites from phytoplankton (dinoflagellates) isolated from different bivalve species (Draisci et al., 1996) and classified into different classes (Liu et al., 2019): Okadaic acid (OA), Dinophysistoxins (DTXs) and Azaspiracids (AZAs) which cause Diarrhetic shellfish poisoning (DSP) (Vale and Sampayo, 2002) and are considered tumor promoters (Fujiki and Suganuma, 1993). These also can cause pathological changes in the liver, pancreas, thymus, and spleen of mice (Ito et al., 2000); while Pectenotoxins (PTXs) and Yessotoxins (YTXs) have not been shown to cause diarrhetic symptoms following intoxication (EFSA, 2008, 2009; Vlamis and Katikou, 2015; Ferron et al, 2016), but Domoic Acid (DA) is a potent neurotoxin responsible for Amnesic shellfish poisoning (ASP) that causes damage to the central nervous system (Gago-Martínez and Rodríguez-Vázquez, 2000; Diogène, 2017).
The Cyclic Imines (CIs)
With the discovery of new detection methods, the toxin groups are constantly updated and new toxins are identified and classified as emerging toxins
. Cyclic Imines (CIs), Palytoxin (PlTX), and Ciguatoxin (CTX) are examples whose appearance in the environment may be due to climate change affecting the distribution of phytoplankton species (EFSA, 2009, 2010a, 2010b). CIs, discovered in Canada in 1991 (Munday, 2008), are associated with algal blooms and shellfish contamination and are neurotoxins, antagonists of nicotinic receptors that affect the central nervous system (Otero et al., 2011). CIs are macrocyclic compounds with 14 to 27 carbon atoms and two highly conserved moieties: the cyclic imine group (mainly a spiroimine) and the spiroketal ring system (Vlamis and Katikou, 2015; Molgó et al., 2017). CIs are exemplified by 40 molecules that differ in the number of their rings: 5-membered (portimines), 6-membered (gymnodimines, spiroprorocentrimines, prorocentrolides), or 7-membered rings (spirolides, pinnatoxins, pteriatoxins), all of which are considered essential components for bioactivity (Stivala et al. 2015 ; Molgó et al., 2017). They were grouped together based on their common imine group (part of a cyclic ring), which is responsible for their pharmacological and toxicological activity, and on their rapid acute toxicity in the mouse intraperitoneal bioassay (EFSA, 2010; Otero et al., 2011; Reverté et al. 2014).
CIs are produced by marine dinoflagellate microorganisms such as Karenia selliformis and Alexandrium ostenfeldii/A. peruvianum, which are associated with the biosynthesis of gymnodimines (GYMs) and spirolides (SPXs) (Seki et al., 1995; Cembella et al., 2000; Touzet et al, 2008; Salgado et al, 2015), while Vulcanodinium rugosum produces pinna toxins and portimines (Nezan and Chomerat, 2011; McCarthy et al, 2015; Molgó et al, 2017), but prorocentrolides were isolated from Prorocentrum lima (Torigoe et al, 1988), spiro- and prorocentrimines are probably produced by Prorocentrum species (Lu et al, 2001).
Poisoning by Marine Biotoxins
Worldwide Cases of Poisoning
According to García et al. (2018), an average of 60,000 people worldwide are poisoned by marine biotoxins each year. Anderson (1989), Quilliam (1993), Anderson (1994, 1997), and Okaichi (2004) have also noted an increase in the frequency and geographic distribution of poisonings worldwide. This high number of cases is attributed to the fact that these toxins are resistant to high temperatures, cannot be smelled, and contaminated seafood appears visually normal (Sobel and Painter, 2005). For example, in Prince Edward Island (Canada) in 1987, 153 deaths were attributed to DA poisoning from the consumption of clams, mussels, oysters, scallops, squid, sardines, anchovies, crabs, and lobsters (Quilliam and Wright, 1993; Lopez-Rivera et al., 2009); and mild memory loss associated with DA has also been observed in Native Americans (Grattan et al., 2016a, b). Seafood poisoning affects not only humans, but also various marine and coastal species that ingest the toxin, such as marine mammals, seabirds, fish, and others (Reyes-Prieto, 2009). Consequently, marine biotoxins do not only threaten ecosystem health, but also affect local economies due to their negative impacts on tourism, recreation, and aquaculture (Morgan ., 2009;et al García
et al., 2016), resulting in economic losses of approximately $82 million (NOAA, 2017; Anderson et al., 2021).
Poisonings in the Mediterranean Sea
Over the past 50 years, a number of HABs have occurred in different areas of the Mediterranean Sea (McNamee et al., 2016). The most recent HAB events were observed in Liguria, Italy, where more than 200 people (tourists and swimmers) experienced various symptoms of illness due to blooms of Ostreopsis ovata (Totti et al., 2010; Ferrante et al., 2013). Also in Italy, mussels contaminated with OA were found in a cultivation area in the Gulf of Trieste, causing poisoning in more than 300 people in 2010 because they were contaminated with various Dinophysis spp. in amounts up to 20 times the legal limit (Bacchiocchi et al., 2015). In addition, several cases of PSP have been reported in different Mediterranean regions such as France, Italy, Morocco, Spain, and Tunisia (Fonda, 1996; Tahri Joutei, 1998; Rhomdane et al., 1998; Taleb et al., 2001; Lilly et all., 2002; EU-NRL, 2002), and mild human ASP poisonings have occurred in Spain, France, Greece, and Italy (Friedman et al., 2008). Although DSP toxins have been found in harvested shellfish in Croatia, no health problems due to the consumption of poisoned seafood have been recorded there (Orhanovic et al. 1996), but severe outbreaks have affected several thousand people in other Mediterranean countries such as France, Greece, and Spain (Belin, 1993; Van Egmond et al., 1993; Durborow, 1999; EU-NRL, 2001; EU-NRL, 2002; FAO, 2004; Ferrante et al., 2013; Costa et al., 2017).
DA occurrence is associated with Pseudo-nitzschia spp. (Sobel and Painter, 2005 ; Ujević et al., 2010 ; Moschandreou et al., 2012) and Nitzschia bizertensis blooms (Bates et al., 2018). This biotoxin was found in wild and cultured bivalve species in Croatia (Ujević et al., 2010), France (Amzil et al., 2001), Greece (Kaniou-Grigoriadou et al., 2005), Italy (Ciminello et al., 2005), and Portugal (Vale and Sampayo, 2001), as well as in Mediterranean lagoons in Tunisia (Sahraoui et al, 2012; Bouchouicha-Smida et al., 2015). Concentrations of DA were below the regulatory limit with a maximum of 6.5486 μg g-1 (detection limit of 0.1025 μg g-1) in mussel samples from the Croatian Adriatic region (Ujević et al, 2010) and below 50 µg g-1 of body weight in France in 2002 (EU-NRL, 2002).
GYMs have been detected in bivalve species, mainly mussels, and clams, in various Mediterranean regions. In Croatia, GYMs were determined at concentrations below the limit of quantification [< 15 μg kg-1] (Gladan et al., 2011; Ujević et al., 2019), while in Greece, concentrations ranged from trace levels to 66 μg kg-1 within the