4. New food sources and food production systems

4.4 Seaweeds

Seaweeds are macroscopic, photosynthetic plant-like organisms that fall under three broad groups based on their pigmentation: brown (Phaeophyta), red (Rhodophyta) and green (Chlorophyta) algae. While the majority of brown and red seaweeds are strictly marine, the green seaweeds are mainly found in freshwater environments (FAO, 2021).

Seaweeds have long been important providers of socioeconomic benefits and contributors to food security (Box 5) around the world through diverse food and non-food applications (FAO, 2021). Though traditionally used as food in various countries (for instance, China, Japan and the Republic of Korea), seaweeds in Western diets have been largely limited to artisanal practices and coastal communities, but has gained wider consumer interest in recent years, driven in part by the health-food industry (Cherry et al., 2019).

Why is seaweed utilization gaining interest?

Two key factors are driving the growing interest in seaweed utilization: heightened attention to sources of food that are nutritious as well as sustainable; and versatility in terms of applications of seaweeds in several industries, such as pharmaceuticals and cosmetics in addition to food and animal feed. Some of these benefits are described below.

Nutritional characteristics

• Human food and potential health aspects: Nutritionally seaweeds consist of minerals (iron, calcium, iodine, potassium, selenium) and vitamins, particularly A, C and B-12. Seaweeds are also one of the only non-fish sources of natural omega-3 long-chain fatty acids. They also tend to be high in soluble dietary fibres, and some can be good sources of protein (FAO, 2018, Gupta and Abu-Ghannam, 2011; Wells et al., 2017).
• Certain bioactive components from various seaweed species have been suggested to confer properties – anti-inflammatory, prebiotic, antioxidant, among others – that are beneficial to health (Joung et al., 2017; Yun et al., 2021). They have also been used as traditional medicines in Asia; for example, some have been used as vermifuge,¹³ and to treat iodine deficiency (Ganesan, Tiwari and Rajauria, 2019; Liu et al., 2012; Moo-Puc, Robledo and Freile-Pelegrin, 2008).
• Animal Feed: Research has shown that the addition of seaweed like Asparagopsis taxiformis to diets of cattle can reduce enteric methane emissions drastically (close to 80 percent) (Kinley et al., 2020; Roque et al., 2019; Roque et al., 2021). Seaweeds can be a sustainable and suitable alternative ingredient in both livestock and aquaculture feeds considering their nutrient profiles, which show species-specific variability (Costa et al., 2021; Kamunde, Sappal and Melegy, 2019; Makkar et al., 2016; Morais et al., 2020; Wan et al., 2019).

Sustainability characteristics

Various varieties of seaweeds not only grow fast, but their cultivation also does not require fertilizers, land degradation or deforestation. In addition, seaweeds provide a number of environmental benefits, some of which are described below.

• Combat ocean acidification – Macroalgae are great carbon dioxide sinks (Duarte et al., 2017). It is estimated that globally seaweeds sequester approximately 200 million tonnes of CO₂ each year, and when they die, much of the trapped carbon gets transported deep into the ocean (Krause-Jensen and Duarte, 2016). This helps to buffer against ocean acidification, which is a consequence of rising atmospheric CO₂ levels. While this property presents an opportunity for climate change mitigation, the current scale of seaweed growth, both from farming and naturally occurring species, is insufficient to support a global role in this endeavour (Duarte et al., 2017).
• Habitat for fish – The seaweeds can provide refuge for various fish species and help to maintain the diversity of marine life. Co-culturing (Box 6) seaweed and shellfish can capitalize on the potential of seaweeds to buffer against acidification, thereby promoting shell calcification of farmed shellfish (Fernández, Leal and Henríque, 2019).
• Prevent eutrophication – In large quantities, nutrients, such as nitrogen and phosphorus, from stormwater runoffs and point-sources cause toxin-producing algal blooms, which have harmful effects on both humans and animals (Anderson, Gilbert and Burkholder, 2002; Heisler et al., 2008). Seaweeds can lower the concentrations of nitrogen and phosphorus in aquatic systems (FAO, 2003) and therefore have potential for wastewater treatment.
• Reduction of pollutants in the area – Macroalgae can accumulate heavy metals from the environment and therefore, could act as bio-monitors to measure the extent of contamination along coastlines (Morrison, Baumann and Stengel, 2008). They can also be cultivated to reduce the levels of heavy metals and other pollutants, thereby improving the health of coastal ecosystems. The seaweeds grown for such purposes should not be used for human or animal consumption.

Seaweeds are a major source of livelihoods and food security in various regions.
©Shutterstock/Ana Flasker

Other noteworthy applications of seaweed include:

• Food additives and non-food applications (agar, carrageenan, and alginates):

• – Thickening/emulsifying agents used in numerous industries including textile, food and beverage, chemical and pharmaceutical, healthcare, and paper.
• – Alternatives for single use plastics: seaweed extracts are being used to make biocompostable packaging for food as well as other articles of single use plastic ware. Few companies around the world are already exploring the possibilities of marketing their technologies on a larger scale.

• Agriculture: There is a growing interest in using seaweeds and their extracts as foliar fertilizers to increase resistance to fungi and insects as well as to serve as sources of nutrition and moisture in the soil (Chojnacka, 2012; Vijayaraghavan and Joshi, 2015). There is also research on capturing the nitrogen run off and returning it back to the farmers to use as fertilizers (Seghetta et al., 2016).

Production estimates of seaweed

The current market value of the global seaweed crop is around USD 5.6 billion, of which sale for human consumption make up the greatest share (FAO, 2020). The main market for seaweed is in Asia and the Pacific, but there growing demand in Europe and North America (FAO, 2020).

Globally fresh seaweed supply comes from two sources: wild stocks and aquaculture (FAO, 2018). Between the two, aquaculture supplies the greater share (Table 3). In 2018, farmed seaweeds represented 97.1 percent by volume of the total of 32.4 million tonnes of wild-collected and cultivated aquatic algae combined (FAO, 2020).

Table 3. Major farmed seaweed producers in the world (thousand tonnes, live weight)

Source: The global status of seaweed production, trade and utilization (FAO, 2018).

Cultivation of microalgae, which are unicellular algal species, is also carried out in various parts of the world for a number of different applications: dietary supplements (Box 7), extraction of bioactive compounds, natural food colourants, and animal feed, among others (FAO, 2021). Production of microalgae can be located in areas that cannot be employed for agriculture, thereby making use of nonarable land (Winckelmann et al., 2015). Microalgae cultivation can also be potentially used for wastewater treatment (Molazadeh et al., 2019; Winckelmann et al., 2015). However, many of these applications are not yet fully commercialized. While further discussion of microalgae is beyond the scope of this brief, as it focuses on macroalgae or seaweeds, the recent FAO publication (2021) has covered the topic of microalgae in greater detail.

What are the food safety implications to be considered?

Given that production of seaweeds is expected to increase globally (Duarte et al., 2017) to meet the rising demand as an alternative source of nutrients, this warrants close attention to the various food safety issues that may arise. Some of the key food safety hazards that should be considered are discussed below.

Microbiological hazards

Microbial contamination can occur during growth, cultivation, harvest, processing and handling, and storage of seaweed. While studies have highlighted that coastal seaweeds can act as reservoirs for Vibrio parahaemolyticus and Vibrio vulnificus populations, the bacterial species are relatively sensitive to heating and drying processes and therefore may not survive the food processing systems (Mahmud et al., 2006; 2007; 2008). However, because seaweed can be consumed raw, microbial risks from such marine foodborne pathogens remain pertinent. Potential risks arising from spore-forming pathogens (Clostridium spp. and Bacillus spp.) are yet to be fully explored.

Outbreaks of foodborne diseases from seaweed can occur if aquaculture farms lack appropriate measures to maintain hygiene and sanitation, such as inadequate facilities for bathroom and handwashing for employees. Location of farms is also important, for instance, if farms are in the vicinity of wildlife refuge (Nichols et al., 2017). Norovirus outbreaks have been linked to seaweed consumption in several countries (EFSA, 2017; Kusumi et al., 2017; Park et al., 2015; Whitworth, 2019).

Chemical hazards

Heavy metals: Seaweeds can bioaccumulate high levels of heavy metals like arsenic, lead, cadmium and mercury from the aquatic environment (Almela et al., 2006; Chen et al., 2018; Karthick et al., 2012; Sartal et al., 2014). These heavy metals can come from both anthropogenic activities (mining, petrochemical processing, electronics waste, municipal waste) and natural causes (volcanic activities). Consumers may be exposed to heavy metals present in seaweed either through direct consumption or indirectly through the food chain, for instance, consuming fish that bioaccumulates the metals by feeding on seaweed. There are a couple of factors that contribute to the process of bioaccumulation: geographical location, especially one with close proximity to a contaminated area; time of harvest, as younger leaves may not contain as much heavy metals as the older leaves; and the intrinsic uptake capacity of the seaweed species concerned (Duncan et al., 2014; Larrea-Marin et al., 2010).

In seaweeds, arsenic can exist in inorganic forms (As^III and As^v) and in its organic forms (monomethylarsonic acid, dimethylarsinic acid, arsenobetaine and arsenocholine) (Francesconi et al., 2004; Rose et al., 2007), with the former considered to be more toxic (McSheehy et al., 2003). While the typical concentration range of As in the oceans range between 1–3 µg l^-1, the total As content (As_T) in seaweeds can be 1 000–50 000 times higher than the surrounding water. Members of Phaeophyta tend to accumulate more arsenic followed by Rhodophyta and Cholorophyta (Ma et al., 2018). There is some evidence to suggest that application of seaweed-based fertilizer to soil may gradually increase the amount of organic and inorganic arsenic concentrations in the treated soil, triggering food safety concerns (Castlehouse et al., 2003).

A range of concentrations has been reported for cadmium in seaweeds intended for human consumption, from below the detection limit (0.001 µg/mL) to 9.8 mg/mL dw (Banach, Hoek-van den Hil and van der Fels-Klerx, 2020). While cadmium has been found to occur at higher levels in red than in brown seaweeds, the case for mercury is the opposite (Chen et al., 2018; Banach, Hoek-van den Hil and van der Fels-Klerx, 2020). Accumulation of lead in brown and green seaweeds was reported by Squadrone et al. (2018) from a location with high anthropogenic activity. According to Almela et al. (2006), the reported lead levels in seaweed range from <0.05 mg/kg to 2.44 mg/kg dry weight. The human exposure to lead from seaweed consumption can be considered minimal (FSAI, 2020).

Iodine content: Iodine is an essential mineral for mammals and is required for biosynthesis of thyroid hormones. While iodine content of seaweeds varies considerably by species, many seaweeds can have significant bioaccumulation capacity for iodine (Nitschke and Stengel, 2015; Roleda et al., 2018). This can result in high mineral content, sometimes up to 100 times higher than terrestrial vegetables (Circuncisão et al., 2018). They are therefore considered iodine-rich foods and depending on volumes consumed could cause excessive intake of the mineral, posing potential health risks (EC SCF, 2002). Post-processing methods can also influence iodine concentrations and therefore human exposure (Dominguez-González et al., 2017; Nitschke and Stengel, 2016).

Women harvesting seaweed.
© Shutterstock/OlegD

Persistent organic pollutants (POPs): Since seaweeds are very low in lipid content, concentrations of lipid-soluble pollutants like dioxins and polychlorinated biphenyls (PCBs) tend to be low (Duinker et al., 2016). However, such chemicals can concentrate in seaweeds if they are grown in areas with high chemical contamination. Dioxins such as polychlorinated dibenzo-p-dioxins (PCDDs) that occur due to industrial contamination (municipal incinerator, power plants, amongst others) have been found in commonly consumed seaweeds such as Undaria and Ecklonia (Banach, Hoek-van den Hil and van der Fels-Klerx, 2020). Also, PCBs have been reported to be absorbed by and concentrated in some seaweeds such as Ulva (Cheney et al., 2014).

Phycotoxins: There are food safety concerns stemming from the potential accumulation of marine toxins (or phycotoxins) by seaweeds. Phycotoxins are produced by harmful microalgal species that can be inadvertently present in areas where seaweeds are harvested from. The growth of filamentous cyanobacteria on edible seaweeds and production of toxins from opportunistic dinoflagellates that can be isolated from seaweed have been flagged as emerging issues of concern (EFSA, 2017; Monti et al., 2007). Risks from algal blooms are of greater concern under climate change-induced conditions (Box 8), such as rising sea temperatures, and ocean acidification.

Some marine toxins such as palytoxin (PTX), domoic acid (DA) and analogs, ciguatoxins, and cyclic imines (CIs) can be found associated with seaweeds (Banach, Hoek-van den Hil and van der Fels-Klerx, 2020). Similarly, ciguatoxin-producing Gambierdiscus toxicus can live in epiphytic association with brown, red and green seaweeds (Cruz-Rivera & Villareal, 2006; FAO, 2004). Various marine sources, including seaweeds, have been reported to cause amnesic shellfish poisoning, which is caused by DA, a potent neurotoxin (FAO, 2004).

Allergenicity: Allergic reactions upon consumption of red seaweeds (Chondrus crispus, Palmaria palmata) were identified by Thomas et al. (2018). However, there is limited information about the allergenic potential of proteins present in seaweeds. In silico proteomic analysis has revealed the allergenic potential of certain algal proteins (aldolase A, thioredoxin h, troponin C, among others) found in Ulva sp. (Polikovsky et al., 2019). Dried nori (Porphyra sp.) has an immunoreactive component (molecular weight 37 kDa) which is identical to the mass of tropomyosin, a known allergen, commonly found in crustaceans (Bito, Teng and Watanabe, 2017). In addition, seaweed is cultivated on long-lines which may be exposed to fouling organisms, including crustaceans, and shellfish allergens are considered a potential hazard in seaweed in the United States of America (Concepcion, DeRosia-Banik and Balcom, 2020).

Other chemical hazards: Agrochemicals such as pesticides and herbicides can enter the marine environment through runoffs from agricultural fields. Monitoring measures will help to establish if these chemicals can enter the food chain through coastal seaweed aquaculture farms. Radionuclides may be a potential hazard from seaweeds harvested from an area that has experienced nuclear incidents, for instance, the 2011 Fukushima incident in Japan (Banach, Hoek-van den Hil and van der FelsKlerx, 2020). According to guideline levels for radionuclides in food set by the Codex Alimentarius, the limits can range from 10 Bq/kg to 10 000 Bq/kg, based on specific radionuclides (FAO and WHO, 2011). The ability of seaweeds to accumulate low levels of radionuclides from the marine environment make them suitable in biomonitoring programmes for radionuclide discharges (Goddard and Jupp, 2001). Seaweeds used for such purposes should not be later used for human or animal consumption.

Pharmaceuticals used both for humans and animals can be found in the marine environment, through sources such as waste disposal, sewage effluent, aquaculture, animal husbandry, among others. Information on the presence of pharmaceutically active compounds in seaweeds is limited. In a study presented by Álvarez-Muñoz et al. (2015), seaweeds Saccharina latissima and Laminaria digitata collected near salmon farm cages showed the presence of four pharmaceutically active compounds, azithromycin (antibiotic), metroprolol (β-blocker), propranolol (β-blocker), and diazepam (psychiatric drug), in levels above the detection limit (Álvarez-Muñoz et al., 2015). Experimental evidence shows that chloramphenicol, furaltadone, and sulfathiazole can be taken up by U. lactuca, with chloramphenicol exerting a potential growth promoter effect on the seaweed (Leston et al., 2011; 2013; 2014).

Seaweeds can utilize nitrogen and nitrogen-derivatives (nitrates) for their biological cycles. While this makes them suitable for capturing and concentrating nitrogen run-offs from agricultural fields, consumption of certain seaweeds may expose consumers to high levels of nitrates (Martin-León et al., 2021). The current acceptable daily intake for nitrate as determined by the Joint FAO/WHO Expert Committee on Food Additives (JECFA) is 3.7 mg/kg body weight per day (FAO and WHO, 2002). Nitrates, from various food sources, can get converted to nitrites in our bodies. Both nitrates and nitrites may contribute to the formation of a group of compounds known as nitrosamines, some of which are carcinogenic (Grosse et al., 2006; Hord, Tang and Bryan, 2009). There is currently no legislation regulating the content of nitrates in seaweeds.

Physical hazards

Physical hazards such as small pebbles and pieces of shells might be present with harvested seaweeds. Processing and packaging of seaweed may introduce other hazards like metal pieces or glass (Concepcion et al., 2020). Micro- and nanoplastics can attach to seaweeds in the aquatic environment, which can then pose potential physical contamination issues down the food chain (Gutow et al., 2016; Li et al., 2020). However, this area has limited information with many knowledge gaps on the occurrence of micro- and nanoplastics in both wild-harvested and cultured seaweeds as well as subsequent health impacts on consumers.

What is the way forward?

Without thorough assessment of food safety risks of seaweeds, developing laws and regulations will be difficult, especially in regions where the sector is just starting to emerge, thereby, impeding progress. While there is global trade of seaweeds, there are no Codex standards or guidelines that specifically address food safety concerns in this food source. Some of the significant gaps in regulations for food safety hazards in seaweeds along with a more detailed overview of the various food safety concerns in seaweeds are captured in an upcoming FAO publication (FAO and WHO, forthcoming).

Upscaling of seaweed production to meet market demand is a challenge for the sector. Long-term data on the environmental impacts of seaweed cultivation at an industrial scale is still lacking. Balancing potential benefits of seaweed production with environmental risks to ensure that the carrying capacities of the receiving environments are not exceeded will be needed. In addition, utmost care must be taken not to introduce non-native species in an area as that might impact the local biodiversity. Implementing a One Health approach to seaweed cultivation will support further development of the sector while ensuring sustainable production and mitigating potential drawbacks (Bizzaro, Vatland and Pampanin, 2022)