Seaweeds: a sustainable food source

CHAPTER

Seaweeds: a sustainable food source

13 Kritika Mahadevan

Food and Consumer Technology, Manchester Metropolitan University, Manchester, UK

1 INTRODUCTION According to the Food and Agricultural Organization (FAO, 2013) and the United Nations (UN, 2014), around 842 million people worldwide suffer from hunger and approximately 2 billion from micronutrient deficiencies. More than 200 million children under the age of 5 years are malnourished. More than 2 billion people, especially in developing countries, are undernourished due to a lack of essential vitamins and minerals. The world population is projected to grow by 20.2% from 2010 to 2030. By 2050, world food production would need to be increased by 60% in order to feed the 9 billion inhabitants. New technologies are being employed in agricultural production, food processing, and packaging to increase food production and reduce waste. The sea is a promising food resource, abundant in seafood including fish and seaweeds (Mahalik and Kim, 2014). Seaweeds are macroalgae that are classified into three groups: brown algae (Phaeophyta), to which wracks/rockweeds (Fucales) and kelps (Laminariales) belong; red algae (Rhodophyta); and green algae (Chlorophyta) (MacArtain et al., 2007). They are found in all coastal areas of the world, from the warm tropics to the cold and icy polar regions. Many of the seaweeds are edible and contain important nutrients such as proteins, essential fatty acids, vitamins, and minerals necessary for human growth and development. Seaweed cultivation is more extensive than other forms of aquaculture including fish farming (Mouritsen, 2013). Around 13 million tons of wet seaweeds are harvested every year in about 40 countries. However, 95% of the total yield comes from China, North and South Korea, Japan, the Philippines, Chile, Norway, Indonesia, United States of America, and India. Approximately 83% of the seaweed produced is used for human consumption (Craigie, 2011). This chapter will explore the role of seaweeds as a sustainable source of food, tracking their usage through history and the future potential of seaweeds as a part of the solution to achieving global food security.

2  HISTORY OF SEAWEEDS FOR HUMAN FOOD Seaweeds have been used as a source of food in the human diet for centuries. They have been an integral part of Asian cuisine in many parts of the world such as Japan, Malaysia, China, and Indonesia. The use of seaweed as food has been tracked back to Seaweed Sustainability. http://dx.doi.org/10.1016/B978-0-12-418697-2.00013-1 Copyright © 2015 Elsevier Inc. All rights reserved.

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the fourth century in Japan and the sixth century in China (McHugh, 2003). Currently, Japan, China, and the Republic of Korea are the largest consumers of seaweed as food. Seaweeds have been used as a food ingredient for many centuries in the western world in places like Iceland, Scotland, Ireland, Maine (USA), Brittany (France), Nova Scotia (Canada), and Wales. Chinese, Japanese, Irish, and Scottish immigrants are likely to have carried the tradition of consuming seaweeds to North America. The oldest documented use of seaweeds for human consumption dates back to 12,000 BCE from a hearth excavated at Monte Verde in southern Chile (Dillehay et al., 2008). Evidence of the presence of about 20 different marine macroalgae, including the genera Porphyra, Gracilaria, Sargassum, Macrocystis, and Durvillaea, has been used by researchers to argue that this part of the South American continent was settled by people who had arrived from the north by following the shoreline rather than by moving inland. Twenty-one different species of edible seaweeds and instructions for their preparation were described in a Japanese–Chinese dictionary dated 934 CE (Mouritsen, 2013). Seaweeds held a very important place in human history in coastal regions since they were seen as hard currency. They were used as a tax contribution in Japan until the eighteenth century, with “nori” and “arame” listed as valuable goods fit for presenting to the emperor. Seaweeds were also used as a trading commodity in Iceland between coastal and inland dwellers since the 700s. Many types of seaweed have been an integral part of the diet in Hawaiian and other Polynesian islands for thousands of years. Mouritsen (2013) observes that at least 40 species of seaweeds were eaten in Hawaii. They were eaten raw, baked, pickled, or mixed with other foodstuffs. The custom of eating seaweed was spread to New Zealand by the Polynesians. Seaweeds like dulse (Palmaria palmate) were likely to have been used in the diet of the costal populations of Ireland more than five millennia back. The first written records stem back to fifth-century Ireland, where dulse was used as a condiment with bread, butter, and milk (Rhatigan, 2009). There are tales about Irish monks in the twelfth century gathering dulse for distribution to the poor and hungry. Ireland maintains a rich tradition of using algae in soups, stews, breads, and salads. In the early 1900s, toasted dulse was served as a snack in Irish and Scottish pubs to stimulate beer consumption. The Irish also widely used the red algae Chondrus crispus that produces a thickening agent called carrageen (Mouritsen et al., 2013). In Brittany, the use of seaweeds as human food goes back at least as far as it does in Ireland. The age-old Breton practice of using dulse and other seaweeds for animal fodder continues to the present. The use of dulse for feeding livestock is also mirrored in terms like cow weed in England and horse seaweed in Norway. In Wales, purple laver (Porphyra umbilicalis) has been eaten since 1600 AD to this day in salads, biscuits, and with roasted meat. It is commonly known as laverbread. In 1607, Camden’s Britannia recorded laver or “lhawvan” being eaten as a survival food from the sea by people in the British Isles forced from their homes during Viking and Roman invasions. George Borrow, in 1865, observed the consumption of laver by the Welsh on his travels through Wales when he mentioned

3 Scope of seaweed as a sustainable source

moor mutton and piping hot laver sauce as one of South Wales’ great dishes. Historically, Welsh laverbread was very important as a nutritious high-energy food source, particularly for hardworking pit workers in the South Wales mining valleys where it became a staple breakfast food (DEFRA, 2014). Women and children working underground in the pits were often malnourished and were advised by doctors to eat Welsh laverbread because it was a very good source of iron. The Inuit of Greenland consumed cooked winged kelp (Alaria esculenta), bladder wrack, dulse, and knotted wrack during the winter (Mouritsen, 2013). In Tasiilaq, an eastern Greenland town, there is an age old tradition of foraging snails and mussels and boiling and eating them with sugar kelp (Saccharina latissima). Written sources such as law codes and sagas, in particular the famous Egil Skallagrimsson’s saga, record the use of seaweeds as human food on Iceland as far back as the tenth century (Mouritsen, 2013). Many different types of seaweeds, mainly red algae, were harvested. According to Mouritsen (2013), Icelanders and possibly also Norwegians ate fresh dulse baked in bread and dried and salted dulse as a snack. For the preparation of a meal, the seaweed was mixed with butter or lard and served with dried, fresh or cooked potatoes and turnips. Another way of preparing dulse was to cook it with milk or put it in porridge. Finally, dulse has also been added to bread dough in order to make the flour stretch further. Food from the sea such as seaweed, fish, and shellfish contains many essential nutrients for sustaining life. Their consumption is believed to have led to the evolution of Homo from the early hominids, resulting in a large brain-to-body weight ratio (Cunnane and Stewart, 2010). Seaweeds are rich in omega-3 fatty acids (docosahexaenoic acid and eicosapentaenoic acid) and minerals such as iodine, iron, copper, zinc, and selenium. These nutrients are necessary for human brain evolution and development.

3  SCOPE OF SEAWEED AS A SUSTAINABLE SOURCE Seaweeds grow in abundance in their natural habitat, in the oceans and seas. Even when farmed, they do not require any manmade fertilizers or water cleaning, thus keeping their environmental impact minimal (Mahalik and Kim, 2014). In addition, they do not compete for agricultural land. Seaweeds have high productivity and reproduce quickly and abundantly when the correct techniques are used. Seaweeds can be consumed in many forms such as raw, dried, or cooked. They are flavorful and packed with nutrients. There are more than 10,000 species of marine algae available in nearly all climatic zones including the warm tropics to the icy polar regions (Mouritsen, 2013). They are nutritionally sustainable, too. For example, the red algae Porphyra can yield 84 g of protein when cultivated in a square meter area. In contrast, a terrestrial protein-rich crop, such as soybean, would provide only 40 g and meat from animals just 5 g/m2. Seaweeds take up only an estimated 8% of the area covered by the oceans. Many of the edible seaweeds have been reported to have a good nutritional composition, making them conducive to a balanced, nutritional

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Table 13.1  Fiber Composition of Seaweeds Compared to Whole Foods Food Type

Total Fiber

Soluble Fiber

Insoluble Fiber

Carbohydrates

8.8

7.5

1.3

13.1

6.2 9.8

5.4 7.7

0.8 2.1

9.9 15

3.4 3.8 5.4 3.8 4.9

2.9 3 3 2.1 2.9

0.5 1 2.3 1.7 2.1

4.6 5.4 10.6 4.1 7.8

Seaweed (g/100 g wet weight)* Ascophyllum nodosum Laminaria digitata Himanthalia elongate Undaria pinnatifida P. umbilicalis P. palmate Ulva sp. Enteromorpha sp.

Whole food (g/100 g weight)† Brown rice Prunes Porridge Lentils green/brown Cabbage Carrots Apples Bananas

3.8 2.4 0.8 8.9 2.9 2.6 2.0 3.1

81.3 19.7 9.0 48.8 4.1 7.9 11.8 23.2

Values for seaweeds from the Institut de Phytonutrition (2004). Values for whole foods from McCance et al. (1993).

*

†

diet. Seaweeds have an abundance of fiber (Table 13.1), minerals, proteins, and carbohydrates (MacArtain et al., 2007) as well as essential fatty acids. All these factors make seaweeds an excellent sustainable food source. Seaweed as whole or seaweed extract can enhance the nutritional properties of processed food products (Prabhasankar et al., 2009b). Along with nutritional benefits, the addition of seaweeds to foods has elicited desirable quality effects by reducing cooking loss, improving texture, etc., as illustrated in Table 13.2. There are some commonly cultivated seaweeds that have been used as a food source for centuries. Since their farming and harvesting methods are well established and they are rich in many essential nutrients, they can form sustainable sources of food. Some popular seaweed consumed by humans is described below.

3.1  “NORI” OR PURPLE LAVER (PORPHYRA SPP.) This is the purplish-black seaweed often seen in sushi wrapped around a small handful of rice. Japan is the largest producer of “nori,” followed by the Republic of Korea

3 Scope of seaweed as a sustainable source

Table 13.2  Application of Seaweed in Bakery and Cereal Products Application Seaweed

Form

Findings

References

Bread

A. nodosum (1, 2, 3, 4%)

Powdered

Hall et al. (2012)

Noodle

Monostroma nitidu (4, 6, 8%)

Powdered

Pakoda

Enteromorpha Powdered compressa (Linnaeus) (5, 7.5, 10, 12.5, 15%)

Pasta

U. pinnatifida (wakame) (5, 10, 20, 30%)

Powdered

Pasta

Sargassum marginatum (1, 2.5, 5%)

Powdered

Beef patty

U. pinnatifida (wakame) (3%)

Dried and ground

Appetite management; significant reduction in total energy in the following 24 h energy intake at subsequent meal test for participants who consumed bread with A. nodosum. The addition of seaweed increased the crude fiber contents of raw fresh noodles. The increase in fiber led to an increase in water absorption. Breaking energy, springiness, extensibility, and viscoelasticity were decreased. Addition of Enteromorpha to pakoda pastry increased iron and calcium contents. Significant increases in dietary fiber, protein, and vitamin contents were observed. However, the free radical-scavenging activity and total phenol content decreased with the addition of Enteromorpha. Starch granules and protein matrix in pasta containing seaweeds up to 20% was shown to be enhanced. Fucoxanthin was not affected by the pasta-making process or the cooking method. The reducing power of the pasta increased with an increased percentage of seaweed in the pasta. Seaweed levels up to 2.5% decreased cooking loss and enhanced the gluten network of the pasta. The inclusion of seaweed decreased thawing and cooking losses and created beef patties with a softer texture. The addition of seaweed also increased the mineral and dietary fiber content.

Chang and Wu (2008)

Mamatha et al. (2007)

Prabhasankar et al. (2009b)

Prabhasankar et al. (2009a)

López-López et al. (2010)

(Continued)

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Table 13.2  Application of Seaweed in Bakery and Cereal Products  (cont.) Application Seaweed

Form

Breakfast sausages

Powdered

Lamina japonica (sea tangle) (1, 2, 3, 4%)

Chicken U. pinnatifida breast meat (wakame) (200 mg/kg meat (w/w))

Restructured Himanthalia poultry steak elongata (sea spaghetti) (3%)

Pork meat emulsion

H. elongata (sea spaghetti), U. pinnatifida (wakame), P. umbilicalis (nori) (5.6%)

Findings

The addition of seaweed at all levels produced no difference in moisture, protein, and fat content. The ash content increased with increasing seaweed content. The 1% seaweed sausages were the most improved for physiochemical and sensory properties. The addition of seaweed Extract carotenoid increased color redness and yellowness in ground pigment, fucoxanthin chicken breast meat. Lipid peroxidation was inhibited in chilling storage after cooking. Powdered Purge loss was slightly increased with the addition of seaweed but cooking losses were reduced. Total viable counts and lactic acid bacteria were of higher levels in the products with seaweed as were the levels of tyramine and spermidine. Dried and Significantly increased the ground omega-3 polyunsaturated fatty acids (PUFA) and decreased the w-6/w-3 PUFA ratio. The seaweed emulsions were significantly lower in sodium than the control. Concentrations of K, Ca, Mg, and Mn increased with the seaweed. Levels of serine, glycine, alanine, valine, tyrosine, phenylalanine, and arginine increased with “nori.” The seaweed increased the antioxidant capacity. The sea spaghetti in particular increased polyphenol supply and antioxidant capacity.

References Kim et al. (2010)

Sasaki et al. (2008)

Cofrades et al. (2011)

López-López et al. (2009a)

3 Scope of seaweed as a sustainable source

Table 13.2  Application of Seaweed in Bakery and Cereal Products  (cont.) Application Seaweed

Cod

Fish

Spice adjunct mix

Form Dried and ground

Findings

The incorporation of algal oil produced frankfurters with high levels of long-chain w-3 PUFA. There were no significant changes in the lipid or amino acid content but it provided the potential for Ca-rich, low-sodium frankfurters with better Na/K ratios while increasing the fiber content. Extract and Phlorotannins from the Fucus subfractions F. vesiculosus extract were vesiculosus shown to inhibit the lipid (Linnaeus) oxidation in fish model (300 mg/kg systems. model) Seaweed could be Kappaphycus Powdered incorporated up to 10% alvarezii without having an effect on (Eucheuma) the appearance, texture, and (5, 7.5, 10, acceptability ratings during the 12.5, 15%) taste panel. Addition of Eucheuma powder Dried and K. alvarezii ground then to the spice adjunct increased (Eucheuma) the ash, protein, and crude (15, 20, 25%) steamed fiber content. It also had a before high amount of vitamin E and using a small amount of niacin and vitamin B2. The addition of Eucheuma up to 20% did not affect its sensory acceptability.

Frankfurters H. elongata (low-fat) (5.5%), algal oil (1.14%)

References López-López et al. (2009b)

Wang et al. (2010)

Senthil et al. (2005)

Senthil et al. (2011)

and China. “Nori” grows as a very thin, flat, reddish blade (McHugh, 2003). In addition to Asia, this seaweed has been used as food for centuries by the indigenous peoples of northwest America and Canada, Hawaii, New Zealand, and parts of the British Isles. It is among the most nutritious seaweeds, with a protein content of 30–50%, and about 75% of that is digestible. Sugars are low (0.1%) and the vitamin content very high, with significant amounts of vitamins A, B1, B2, B6, B12, C, niacin, and folic acid. It contains 10 times as much vitamin A as spinach. However, the vitamin C content can decrease by drying the product. “Nori” sheets are low in sodium since most of the salt is washed away during processing. The characteristic taste of “nori” is caused by large amounts of three amino acids: alanine, glutamic acid, and glycine. “Nori” is used mainly as a luxury food. As mentioned previously, it is often used in sushi, wrapped around a small portion of boiled rice with a slice of raw fish on the

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top. In recent times, vegetarian sushi has also become popular to reach more consumers. Toasted “nori” can be cut into small pieces and sprinkled over boiled rice or noodles or added to soups, bread, and salads. It can be incorporated into soy sauce and boiled down to give an appetizing luxury sauce. It is also used as a raw material for jam and wine. In China it is mostly used in soups and for seasoning fried foods. In the Republic of Korea it has similar uses to Japan, except that a popular snack with beer is “hoshi-nori” that has been quickly fried in a pan with a little oil.

3.2  “AONORI” OR GREEN LAVER (MONOSTROMA SPP. AND ENTEROMORPHA SPP.) These two green seaweed genera are cultivated in Japan. Monostroma latissimum occurs naturally in the bays and gulfs of southern areas of Japan. It is a flat, leafy plant and only one cell thick. It contains 20% protein on average and has a useful vitamin and mineral content. The seaweed is washed well postharvest. It is then either processed into sheets and dried, as described for Porphyra, or dried and then boiled with sugar, soy sauce, and other ingredients to make “nori-jam.” Enteromorpha prolifera and Enteromorpha intestinalis (McHugh, 2003) are both cultivated and are found in bays and river mouths around Japan. They are also found in many other parts of the world, including Europe and North America. They contain about 20% protein and are low in fat and sodium and high in iron and calcium. The vitamin B group content is generally higher than most vegetables, and while its vitamin A content is high, it is only half of that found in spinach. The seaweed can be lightly toasted to improve the flavor and powdered for use as a condiment on soups and foods, or it can be crushed into small pieces and used as a garnish. Sea lettuce is a thin, green seaweed, a species of Ulva. It is collected from the wild and sometimes added to the above two seaweeds as part of “aonori,” which enhances the taste of warm dishes like rice, soups, and salads. It has a higher protein content than the other two and is rich in iron. However, it has a much lower vitamin content, except for niacin, which is double that of Enteromorpha (McHugh, 2003)

3.3  “KOMBU” OR “HAIDAI” (LAMINARIA JAPONICA) “Kombu” is the Japanese name for the dried seaweed that is derived from a mixture of Laminaria species. These include L. longissima, L. japonica, L. angustata, L. coriacea, and L. ochotensis. Haidai is the Chinese name for L. japonica, introduced to China accidentally from Japan in the late 1920s. Previously, China imported all its requirements from Japan and the Republic of Korea. It is now cultivated on a large scale in China. It is a large seaweed, usually 2–5 m long, but it can grow up to 10 m in favorable conditions (McHugh, 2003). Laminaria species contain about 10% protein, 2% fat, and useful amounts of minerals and vitamins, though generally lower than those found in “nori.” For example, they have one-tenth the amount of vitamins B2, B12, and niacin and half the

3 Scope of seaweed as a sustainable source

amount of B1 but three times the amount of iron as compared with “nori.” Brown seaweeds also contain iodine, which is lacking in “nori” and other red seaweeds. In China, haidai is regarded as a healthy vegetable because of its mineral and vitamin content. In Japan, it is used in everyday food, such as a seasoned and cooked “kombu” that is served with herring or sliced salmon. “Kombu” tea is like green “kombu” but is shaved a second time so that the shavings are like tea leaves. “Kombu” is boiled with meat, fish, and soups and added to sauces and rice.

3.4  “WAKAME,” “QUANDAI-CAI” (UNDARIA PINNATIFIDA) Wakame is the Japanese name for the brown seaweed U. pinnatifida, and it is a type of kelp. It has a sweet, mild taste. It can be consumed toasted, cooked for a short while to make “miso” soup, or soaked in water to make salad. It grows in Japan, the Republic of Korea, China, France, New Zealand, and Australia. Wakame has an attractive dark greenish-brown color and has a high total dietary fiber content, higher than “nori” or “kombu.” Like the other brown seaweeds, the fat content is quite low, but it is rich in omega-3 fatty acids (Mouritsen, 2013). Air-dried wakame has a similar vitamin content to wet seaweed and is relatively rich in the vitamin B group, especially niacin; however, processed wakame products lose most of their vitamins. Raw wakame contains appreciable amounts of essential trace elements such as manganese, copper, cobalt, iron, nickel, and zinc, similar to “kombu” and “hiziki.”

3.5  “HIZIKI” (HIZIKIA FUSIFORME) These brown algae grow in the wild shallow waters by the coast of China, Korea, and Japan. Postharvest, they are sun dried, boiled in a lot of water to remove arsenic, and dried again to produce a black product. Due to the arsenic content, government food safety agencies in many countries have warnings against consuming this seaweed in large quantities. The protein, fat, carbohydrate, and vitamin contents are similar to those found in “kombu,” although most of the vitamins are destroyed in the processing of the raw seaweed (McHugh, 2003). The iron, copper, and manganese contents are relatively high, certainly higher than in “kombu.” Like most brown seaweeds, their fat content is low (1.5%), but 20–25% of the fatty acid is eicosapentaenoic acid. Typically, it is stir fried with fried bean curd and vegetables such as carrot, or it may be simmered with other vegetables. It has a pleasant, firm texture and a mild, nutty taste and can be incorporated into salads.

3.6  DULSE (PALMARIA PALMATA) Dulse, a red algae, is harvested in Ireland, on the eastern coast of Canada, and in Maine. Dried dulse is broken into flakes or ground into powder for use as a seasoning. It is sometimes added to corn chips. In Nova Scotia and Maine, dried dulse is often served as a salty cocktail snack in bars. It is eaten raw in Ireland, like chewing

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tobacco, or is cooked with potatoes, in soups, and fish dishes. In present day cuisine, dulse can be incorporated into bread, fish dishes, fish and vegetable soups, toasted and eaten as a snack, or fried crisp as a substitute for fried bacon. Dulse is a good source of minerals, being very high in iron and containing all the trace elements needed in human nutrition. Its vitamin content is also much higher than a vegetable such as spinach. It has high protein content (more than 20%) but lacks the essential amino acid tryptophan (Mouritsen, 2013). Of all the marine algae, dulse has a flavor more agreeable to the western palate.

3.7  MOZUKU (CLADOSIPHON OKAMURANUS) This brown seaweed is harvested from natural populations in the more tropical climate of the southern islands of Japan. The harvested seaweed is protected from sunlight, cleaned, salted, and sold in wet form. After washing to remove the salt, it is used as a fresh vegetable, eaten with soy sauce and in seaweed salads.

3.8  SEA GRAPES OR GREEN CAVIAR (CAULERPA LENTILLIFERA) There are many species of the genus Caulerpa, but Caulerpa lentillifera and C. racemosa are the two most popular edible ones. Both have a grape-like appearance and are used in fresh salads. They are cultivated in the central Philippines and exported to Japan (McHugh, 2003).

3.9  IRISH MOSS OR CARRAGEENAN MOSS (C. CRISPUS) Irish moss has a long history of use in foods in Ireland and some parts of Europe. It is not eaten as such but is used for its thickening powers when boiled in water, a result of its carrageenan content. It is used to make puddings, incorporated in seaweed salads, as sashimi garnishes, and as a soup ingredient.

3.10  WINGED KELP (A. ESCULENTA) This large, brown kelp is found in areas such as Ireland, Scotland, Iceland, Brittany, Norway, Nova Scotia, Sakhalin (Russia), and northern Hokkaido (Japan). It is eaten either fresh or cooked. It is said to have the best protein among the kelps and is also rich in trace metals and vitamins, especially niacin, vitamin A, and calcium. Dried winged kelp is rehydrated in cold water before using it in food items like salads. It has a mild taste. The midrib can be eaten after toasting and when deep-fried the sporophylls taste like peanuts.

3.11  “OGO,” “OGONORI,” OR SEA MOSS (GRACILARIA SPP.) Fresh Gracilaria has been collected and sold as a salad vegetable in Hawaii for several decades. In Indonesia, Malaysia, the Philippines, and Vietnam, species of Gracilaria are collected by coastal people for food. In southern Thailand, an education

4 Seaweeds in the food chain

program was undertaken to show people how it could be used to make jellies by boiling and making use of the extracted agar. In the West Indies, Gracilaria is sold in markets as sea moss; it is reputed to have aphrodisiac properties and is also used as a base for a nonalcoholic drink. It has been successfully cultivated for this purpose in St Lucia and adjacent islands (McHugh, 2003).

3.12  CALLOPHYLLIS VARIEGATA In Chile, the demand for this red, edible seaweed has increased dramatically. It is commonly known as carola.

3.13  BLADDER WRACK (FUCUS SPP.) Bladder wrack is a brown algae from the genus Fucus. It is widespread along the coastlines of most parts of the world. The best-known bladder wrack is F. vesiculosus (Mouritsen, 2013). Some varieties of bladder wrack are used to make a tea and can be used in the same way as “kombu” (Japanese kelp). The youngest and outermost shoots of the seaweed are very tasty. Fucus is dried and sold as granules or as small branches. It has a strong iodine taste and is very salty. It can be incorporated in cooked dishes and soups and sprinkled in salads.

3.14  SEA PALM (POSTELSIA PALMAEFORMIS) These brown algae resemble a small palm tree. They grow on the west coast of North America from central California to British Columbia. They are regarded as a threatened species. In California, their harvest is allowed for limited commercial use (Mouritsen, 2013). Sea palm blades are eaten and they are very rich in fiber (65%). They can be dried, toasted, and eaten as snacks. They can be cooked, marinated, and used in salads.

3.15  ARAME (EISENIA BICYCLIS OR EISENIA ARBOREA) These brown algae are harvested along the Pacific coast of Japan. They are rich in calcium, which is in chelated form. Hence, the body can absorb more of the calcium easily in this form. It is first sun dried, then steamed or boiled for several hours, cut into strips, and dried once more. It rehydrates in 5 min but will lose flavor if left in water for too long. Arame is milder and less salty than haziki. It is one of the sweetest seaweeds commonly consumed. It can be used in salads, soups, and marinated.

4  SEAWEEDS IN THE FOOD CHAIN Seaweeds and their extracts play an important part in the food chain. They form a favorable ecosystem for the survival of many organisms in the seas and oceans that end up eventually as human food. They act as food for both small and large marine

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animals. Small bits of marine algae are consumed via filter feeding by krills, bivalves, sponges, and whale sharks. Snails, sea urchins, and herbivorous fish like carp and tilapia eat seaweeds directly (Mouritsen, 2013). Slime secretions from seaweeds, which are rich in polysaccharides, simple sugars, and amino acids, are ingested by sponges, bacteria, and other unicellular aquatic organisms. When these organisms are consumed by marine carnivores, the nutrients from the seaweeds move higher up the food chain. In recent times, seaweed protein has been extracted and used as fish feed. In Australia, the brown seaweed Macrocystis pyrifera and the red seaweed Gracilaria edulis have been used as abalone feed (McHugh, 2003). In South Africa, Porphyra is in demand for abalone feed. Pacific dulse (Palmaria mollis) has been found to be a valuable food for the red abalone, Haliotis rufescens. In addition to being a source of food, seaweeds play a major ecological role as a safe habitat for invertebrates, fish, mammals, and birds (Graham et al., 2007). They serve as nursery sites and hiding places for fish fry and shellfish. Seaweeds have been used as fertilizer for plants or as feed for animals. For hundreds of years, seaweed and seaweed compost have been used as fertilizer in coastal regions. Brown algae have been used as fertilizer in France since 1300. Seaweeds have been used as fertilizer in vineyards, too (Mouritsen, 2013). Coastal dwellers have used storm-cast seaweed as fertilizer for years by digging it into the soil. The high fiber content of the seaweed acts as a soil conditioner and aids in moisture retention. The nutrients from the seaweed such as minerals and trace elements enrich the soil. Organic growers have used seaweeds to fertilize and mulch beds to grow vegetables like asparagus that are salt tolerant. The seaweeds are washed in rainwater to remove any external salt from the seawater that can make the soil saline. Seaweed extracts in liquid form are being researched and used as plant fertilizers and growth stimulants. When used diluted at low concentrations, liquid fertilizers derived from seaweed were found to be better than chemical fertilizers (Arun et al., 2014). They are highly nutritious and with organic credential; they also promote seed germination and increase the yield of many plants used as human food. Due to their nutritional value, seaweeds have been used as animal fodder for domesticated animals. There are written records from the first century CE of cattle being fed seaweeds in the Mediterranean basin (Mouritsen, 2013). Different species of marine algae have been used to feed domestic animals when there was scarcity of grass throughout the Middle Ages on the coastlines of Iceland, the Faroe Islands, ­Ireland, Greenland, and Norway. Sheep in the Orkneys still consume seaweed and their mutton is famed for its special salty flavor. Feeding trials that incorporated seaweed meal made from A. nodosum showed an increase in the iodine content of the eggs in the poultry that consumed the feed. In the case of dairy cows, increases in milk production were observed, while sheep were able to maintain weight better during winter feeding, with increases in lambs’ birth weights and greater wool production (Holdt and Kraan, 2011).

5 Safety around seaweed consumption

5  SAFETY AROUND SEAWEED CONSUMPTION There are no daily recommendations for the intake of seaweeds. Five to eight grams of dry weight seaweed is a typical daily portion size consumed in Asian cuisine (MacArtain et al., 2007; Mouritsen, 2013) and therefore can be used as a safe recommendation. This would correspond to 30–50 g of wet seaweed. In most countries, there are no special regulations enforced for the use of seaweeds and algae as human food. The intakes have to conform to the general safety regulations for food and its contents, specified by a provisional tolerable weekly intake recommended by the World Health Organization based on an average adult body weight of 68 kg. However, France has a specific list of seaweeds (Table 13.3) for human consumption (Mabeau and Fleurence, 1993; Burtin, 2003). While edible seaweeds are rich in nutrients, some species accumulate heavy metals from their environment. Such undesirable metals and compounds can be harmful when consumed by humans and animals. Therefore, if seaweed species are to be used as food product or animal feed, they should be tested for metals in inorganic and organic form. The concentrations of heavy metals in seaweeds depend on many factors, mainly bioavailability of metals in the surrounding water and the uptake capacity of the algae (Besada et al., 2009). France specifies upper limits for the contents of inorganic arsenic, lead, cadmium, tin, mercury, and iodine in edible seaweeds (Table 13.4). When 11 commercialized food samples from Spain containing nine seaweed species were studied by Besada et al. (2009), the samples exceeded the limits set for cadmium. H. fusiforme showed the largest total and inorganic arsenic concentrations, in all cases exceeding the inorganic arsenic limit specified by France. In contrast, another study determined very low concentrations of heavy metals in edible seaweeds in South Korea (Khan et al., 2015) that would pose no threat to consumers. While there are no specific restrictions posed on human consumption of most edible seaweeds, the European Union has legislation in place for the cultivation and harvesting of seaweeds, as well as the approval and usage of extracts and bioactive compounds from seaweeds (EU, 2009). Japan has specifications under the “functional foods” category. A comprehensive review of legislation from the European Union, United States of America, and countries like Japan along with health claims legislation was published by Holdt and Kraan (2011). The Tolerable Upper Intake Level is defined as the highest level of daily intake that is likely to pose no adverse health Table 13.3  Seaweed Authorized for Human Consumption in France Brown Seaweed

Red Seaweed

Green Seaweed

A. nodosum Fucus serratus Fucus vesiculosus Himanthalia elongata U. pinnatifida

P. umbilicalis Palmaria palmata C. crispus Gracilaria verrucosa

Enteromorpha spp. Ulva spp.

Source: Burtin (2003).

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Table 13.4  Quality Criteria Applied to Edible Seaweed Sold in France (Burtin, 2003), Regulations in the US (Mabeau and Fleurence, 1993), and for Dietary Supplements in the EU (2008) Limit (mg/kg Dry Matter, ppm) Toxic Minerals

France

US

EU Regulation

Inorganic arsenic Lead Cadmium Tin Mercury Iodine Heavy metals

<3.0 <5.0 <0.5 <5.0 <0.1 <0.5

<3.0 <10

No regulation <3.0 <3.0 <0.1

<5000 <40

effects in most human individuals. In most instances, regular consumers of seaweed products would not reach these amounts. Due to high concentrations of inorganic arsenic found in H. fusiforme, a daily consumption of 1.7 g of the product would be advisable and within the tolerable weekly intake (Almela et al., 2002).

6  CHALLENGES AND OPPORTUNITIES There has been an increase in the popularity of seaweed-based foods even in places where it has not been traditionally consumed due to the increase in travel and exposure to different cuisines globally. Additionally, consumers are more interested in eating healthily and using whole foods from basic sources. Chefs are increasingly showcasing interesting seaweed cuisine, thus incorporating various species of seaweeds into foods (Mouritsen et al., 2013). In order to establish seaweed as a sustainable food source, it will need to be more widely consumed globally and not just in Asia. There is a plethora of recipe books showcasing gourmet cooking with seaweeds, often renamed as “sea vegetable” to make it sound appealing. Some people subscribe to these cookbooks. However, seaweed would need to be incorporated into an increasing variety of foods readily available to the global population. The key challenge faced by the food industry is in making foods containing seaweed more desirable to the global consumer. Some strategies used include creating foods that are organoleptically acceptable to the consumer based on the flavor and textural properties. Another popular strategy is enhancing the nutritional and health benefits of popular foods such as bread and pasta with the addition of seaweeds or their extracts. Incorporation of the brown seaweed A. nodosum into bread was shown to produce an organoleptically acceptable product that led to a significant reduction in the energy intake in overweight males (Hall et al., 2012). The red seaweed P. palmata is commonly found in Europe and America and is rich in protein content (9–25%, depending on the time of harvest). Protein

7 Conclusions

hydrolysate from this seaweed was enriched in renin inhibitory peptides by Fitzgerald et al. (2014), which can help to prevent cardiovascular disease. These peptides were successfully incorporated into bread, which acted as a carrier for this bioactive ingredient (Fitzgerald et al., 2014). The ecosystems of the oceans are worth an estimated 25,000 billion US dollars and the marine algae/sea grasses have a value that is greater than the rainforests and coral reefs together (Mouritsen, 2013). The marine world offers great opportunities financially, which has been a reason for a good number of companies that have embarked on cultivating seaweeds commercially. For example, the seaweed dulse (P. palmata) is harvested, dried, packed, and sold commercially by many small enterprises in Ireland, Brittany, Spain, Iceland, Maine, Nova Scotia, and California. Commercial cultivation of the seaweed takes place in a large scale in the open sea by the northern Spanish coastline (Martínez et al., 2006). Cultivation of seaweed can be a profitable activity, especially for coastal communities because it has a short production cycle, low capital requirement, and relatively simple farming technology. The challenges that would need to be overcome include seasonality and variability in the nutritional composition of seaweeds, disease, inclement weather, and competition. The life cycle assessment (LCA) on kelp aqua farming in Chile indicated that the energy returns on seaweed cultivation were positive (Buschmann, 2014). LCA is an assessment tool of the environment regarding waste, losses of raw material, and usage of the environment during production – for example, water resources, soil, contribution to climate change, eutrophication, and decrease in biodiversity (Gandini et al., 2009). This approach helps to identify the parts of the production chain where further technological development is required with the aim of reducing the environmental impact. As seaweed cultivation and consumption increases worldwide, LCA and the environmental impact should also be monitored over time to ensure the sustainable growth and utilization of seaweeds as a food source.

7 CONCLUSIONS Edible seaweeds have the potential to be a very good source of sustainable food. They are rich in many of the essential nutrients required for healthy living. They grow in abundance naturally and can be harvested from the sea. They can also be cultivated in the oceans, seas, and in pools inland with minimal environmental impact. Eating more marine algae could be a part of finding sustainable ways to enhance food and nutritional security. The oceans are an abundant natural resource not yet fully utilized. However, this would require research and development of technologies for cultivating, harvesting, and processing various varieties of seaweeds while respecting the ecological cycles of the oceans. Utilization of seaweeds as a sustainable food source would also require promoting them for human consumption in the developed and developing worlds through innovation and identification of niche markets.

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