Seaweeds in the human diet as an alternative to achieve the Sustainable Development Goals: A risk-benefit approach

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Seaweeds in the human diet as an alternative to achieve the Sustainable Development Goals: A risk-benefit

approach

Maria Beatriz Marta Ferreira de Jesus Fernandes

DEPARTAMENTO DE CIÊNCIAS E ENGENHARIA DO AMBIENTE

MESTRADO INTEGRADO EM ENGENHARIA DO AMBIENTE - Perfil de Engenharia de Sistemas Ambientais

Universidade NOVA de Lisboa

Licenciada em Ciências de Engenharia do Ambiente

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DEPARTAMENTO DE CIÊNCIAS E ENGENHARIA DO AMBIENTE

Seaweeds in the human diet as an alternative to achieve the Sustainable Development Goals: A risk- benefit approach

Orientadora: Marta Susana Silvestre Gouveia Martins,

Professora Auxiliar, NOVA School of Science and Technology

Coorientador: Ricardo Assunção, Professor Auxiliar, Instituto Universitário Egas Moniz (IUEM), Egas Moniz – Cooperativa de Ensino Superior, CRL

Júri:

Presidente: Professora Doutora Maria da Graça Madeira Martinho Professora Associada com Agregação, NOVA School of Science and Technology

Arguente: Doutora Sara Neves da Costa Monteiro Pires

Senior Researcher, National Food Institute - Technical University of Denmark

Vogal: Professora Doutora Marta Susana Silvestre Gouveia Martins Professora Auxiliar, NOVA School of Science and

Technology

Maria Beatriz Marta Ferreira de Jesus Fernandes Licenciada em Ciências de Engenharia do Ambiente

MESTRADO INTEGRADO EM ENGENHARIA DO AMBIENTE Universidade NOVA de Lisboa

Janeiro, 2022

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Seaweeds in the human diet as an alternative to achieve the Sustainable Development Goals: A risk-benefit approach

A Faculdade de Ciências e Tecnologia e a Universidade NOVA de Lisboa têm o direito, perpétuo e sem limites geográficos, de arquivar e publicar esta dissertação através de exemplares impressos reproduzidos em papel ou de forma digital, ou por qualquer outro meio conhecido ou que venha a ser inventado, e de a divulgar através de repositórios científicos e de admitir a sua cópia e distribuição com objetivos educacionais ou de investigação, não comerciais, desde que seja dado crédito ao autor e editor.

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ACKNOWLEDGMENTS

First of all, I would like to thank Professor Marta for all the guidance and support provided throughout this great and last stage of my academic journey. Thank you for having figured out from the start which path would be the best way to go.

To Dr. Ricardo, for all his availability and knowledge transmitted throughout my dissertation. It was undoubtedly a fundamental help in this project.

I want to thank my mother, Sofia, and my father, João, for all their love. For always believing in me and always having the right word, at the right time, to tell. They are definitely the best in the world.

To Venas, Marta, Pipa, and Gui, my colleagues and friends, for being by my side and making this adventure easier and more enjoyable. To my favourite freshman girls Bea and Catarina, for having been fundamental in this path too.

To Ana, for all the patience she had for me throughout this phase. Thanks also for all the strong words in my most dramatic moments.

To my remaining family, grandparents, uncles, and cousins, because all of them, in some way, were part of my path. Thank you all.

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ABSTRACT

The existence of various inequalities at the world level makes it difficult to achieve the sustainable development. In order to change this paradigm, increasingly ambitious goals are emerging, such as the Sustainable Development Goals (SDGs), as well as new alternatives to achieve them more quickly. Seaweeds have been identified as a potential solution to this problem due to their important role in providing various ecosystem services as well as their nutrient richness. As a result, in this Thesis, a risk-benefit assessment (RBA) was performed for the consumption of two macroalgae species: Porphyra sp. and Undaria pinnatifida. For this RBA, and in order to analyse the benefits associated with the consumption of these two species, the amounts of nutrients present in both were compared with the dietary reference values (DRV) for the adult population. To assess the risk component associated with their consumption, an analysis of the contaminants frequently present in these algae was conducted, based on the methodologies applied by the European Food Safety Authority (EFSA) in different studies for each element. The results of this RBA, together with the literature gathered throughout this Thesis, allow the connection between the consumption and production of seaweeds with the achievement of several targets of the SDGs, as well as the potential achievement of other targets.

Keywords: Seaweed, risk-benefit assessment, nutrition, toxicology, health, sustainable development goals

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RESUMO

A existência de várias desigualdades a nível mundial dificultam o objetivo de atingir o desenvolvimento sustentável. De forma a alterar este paradigma, vão surgindo metas cada vez mais ambiciosas, como é o caso dos Objetivos de Desenvolvimento Sustentável, bem como novas alternativas para mais rapidamente os atingir. Devido ao seu importante papel ao nível do fornecimento de vários serviços ecossistémicos, assim como à sua riqueza nutritiva, as algas têm sido apontadas como uma boa solução para minimizar este problema.

Assim sendo, nesta Tese, foi realizada uma avaliação risco-benefício (ARB) para o consumo de duas espécies de macroalgas: Porphyra sp. e Undaria pinnatifida. Para esta avaliação, e de forma a analisar os benefícios associados ao consumo destas duas espécies, as quantidades dos nutrientes presentes em ambas as espécies foram comparadas com os valores recomendados para a população adulta. Para avaliar a componente de risco inerente ao consumo das duas espécies de algas, os contaminantes frequentemente presentes para estas algas foram analisados com base nas metodologias aplicadas pela Autoridade Europeia para a Segurança Alimentar (EFSA) em diferentes estudos, de acordo com cada elemento. Os resultados obtidos para esta ARB, juntamente com a literatura recolhida ao longo deste trabalho, permite relacionar o consumo e a produção de algas, ao cumprimento de várias metas dos objetivos de desenvolvimento sustentável, sendo possível ainda verificar o potencial para o cumprimento de outras.

Palavras-chave: Algas, avaliação do risco-benefício, nutrição, toxicologia, saúde, objetivos de desenvolvimento sustentável

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LIST OF ABBREVIATIONS

AI Adequate Intake AR Average Requirement BMD Benchmark Dose

BMDL Benchmark Dose (Lower Confidence Limit) BW Body weight

DRV Dietary Reference Value

EFSA European Food Safety Authority EU European Union

FAO Food and agriculture organization FS Food System

GHG Greenhouse gases

IMTA Integrated multi-trophic aquaculture ML Maximum Levels

MOE Margin of exposure

OIE World Organization for Animal Health PA Polyamide

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PE Polyethylene

PET Polyethylene terephthalate PP Polypropylene

PRI Population reference intake RBA Risk-Benefit assessment RBQ Risk-Benefit question

SDG Sustainable Development Goals Sp. Species

Spp. Species (plural form) TWI Tolerable weekly intake UL Tolerable upper intake level UN United Nations

WHO World Health Organization

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LIST OF FIGURES

FIGURE 1-GLOBAL PRODUCTION OF MACROALGAE BASED ON AQUACULTURE (ADAPTED FROM EUROPEAN

COMMISSION,2019). ... 8

FIGURE 2-GLOBAL WILD HARVESTING OF MACROALGAE (ADAPTED FROM EUROPEAN COMMISSION,2019). . 9

FIGURE 3-EXAMPLE OF A STRUCTURE BASED ON THE OFF-BOTTOM TECHNIQUE (SOURCE:ROBLEDO ET AL., 2013). ... 10

FIGURE 4-EXAMPLE OF A STRUCTURE BASED ON THE FLOATING SYSTEM TECHNIQUE (SOURCE:ROBLEDO ET AL.,2013). ... 11

FIGURE 5-PRODUCTION EVOLUTION OF KAPPAPHYCUS ALVAREZII,EUCHEUMA DENTICULATUM,GRACILARIA VERRUCOSA,SACCHARINA JAPONICA,PORPHYRA SPP., AND UNDARIA PINNATIFIDA OVER THE YEARS. .. 16

FIGURE 6-RISK-BENEFIT ASSESSMENT PARADIGM.ADAPTED FROM EFSA(2010) AND THOMSEN (2018). ... 22

FIGURE 7–RISK-BENEFIT ASSESSMENT APPROACH (ADAPTED FROM ASSUNÇÃO ET AL.2019). ... 35

FIGURA 8-UNDARIA PINNATIFIDA (SOURCE:ZAIXSO,H.,&BORASO,A.(EDS.),2014)... 36

FIGURE 9-PORPHYRA TENERA (SOURCE:FAO,2021A). ... 37

FIGURE 10–PERCENTAGE OF THE DAILY NUTRIENT REQUIREMENTS SATISFIED BY THE CONSUMPTION OF PORPHYRA SP. AND UNDARIA PINNATIFIDA SPECIES, FOR THE REFERENCE SCENARIO. ... 47

FIGURE 11–EXPECTED INTAKE OF IODINE FROM THE CONSUMPTION OF PORPHYRA SP. AND UNDARIA PINNATIFIDA, FOR EACH OF THE SCENARIOS CONSIDERED (REFERENCE SCENARIO;4 G;SCENARIO 1:2 G; SCENARIO 2:10 G).THE GREEN LINE INDICATES ADEQUATE INTAKE (AI), AND THE RED LINE INDICATES UPPER INTAKE LEVEL (UL). ... 48

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LIST OF TABLES

TABLE 1-IDENTIFIED PROS AND CONS, ASSOCIATED WITH THE FOUR TYPES OF SEAWEED PRODUCTION. ... 15 TABLE 2-ACTIONS RESULTING FROM THE PRODUCTION AND CONSUMPTION OF SEAWEEDS, AND RESPECTIVE

POTENTIAL GOALS AND TARGETS TO BE ACHIEVED AS A CONSEQUENCE OF THESE ACTIVITIES. ... 24 TABLE 3-FOOD COMPOSITION OF PORPHYRA SP. AND UNDARIA PINNATIFIDA SPECIES BASED ON VALUES

AVAILABLE IN THE FRENCH FOOD COMPOSITION TABLE (SOURCE:ANSES-CIQUAL,2021B;ANSES- CIQUAL,2021C).THE INDICATED VALUES CORRESPOND TO THE AMOUNT OF NUTRIENTS PRESENT IN 100 GRAMS OF SEAWEED. ... 42 TABLE 4-DIETARY REFERENCE VALUES OF SELECTED NUTRIENTS (SOURCE:DRVFINDER,2021)... 42 TABLE 5–CONTAMINANTS FOUND IN PORPHYRA AND UNDARIA SPECIES, IN STUDIES CARRIED OUT ON THE

PORTUGUESE COAST. ... 43 TABLE 6–MARGIN OF EXPOSURE (MOE) VALUES FOR INORGANIC ARSENIC, WHEN APPLIED A CONVERSION

FACTOR OF 1%, ACCORDING WITH THE THREE DIFFERENT SCENARIOS. ... 50 TABLE 7–MARGIN OF EXPOSURE (MOE) VALUES FOR INORGANIC ARSENIC, WHEN APPLIED A CONVERSION

FACTOR OF 70%, ACCORDING WITH THE THREE DIFFERENT SCENARIOS. ... 50 TABLE 8–DAILY AND WEEKLY VALUES OF EXPOSURE TO CADMIUM, ACCORDING WITH THE THREE

CONSIDERED SCENARIOS. ... 51 TABLE 9–MARGIN OF EXPOSURE (MOE) VALUES FOR LEAD, USING AN BMDL10 OF 0.63 µG/KG B.W./DAY

AND A BMDL01 OF 1.5 µG/KG B.W./DAY. ... 52 TABLE 10–DAILY AND WEEKLY ESTIMATED VALUES OF EXPOSURE TO MERCURY, ACCORDING WITH THE

THREE CONSIDERED SCENARIOS. ... 53

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1. Introduction

According to the United Nations (UN) (1987), the sustainable development can be defined as the “development that meets the needs of the present without compromising the ability of future generations to meet their own needs”. To ensure this sustainable development, three fundamental pillars must be considered in an integrated manner:

economic growth, social inclusion, and environmental protection (UN, 2021a). Despite joint efforts to achieve this development, several aspects reveal that there is still a long way to go in this direction.

The Report on the World Social Situation 2013, developed by the UN, among several themes, discusses inequalities in health, education, and economics. In this report, it is clear that these inequalities still accentuated in certain aspects – for example, the disparity in life expectancy which, despite having decreased in most regions, was not observed for Sub- Saharan Africa; the likelihood of attending school which varies by gender and location; or even the difference between the income of developed and non-developed countries (UN, 2013). Concerning the environment, the scenario is also unsatisfactory. For example, the 2014 IPCC Report states that since 1950 there have been changes in various extreme events related to climate, part of which have been associated with anthropogenic causes. In addition, the same report states that the effects associated with extreme climate-related events (e.g., droughts, floods, heatwaves, and forest fires) lead to changes in ecosystems, impairment of food production, failure in water supply, infrastructure damage, morbidity, mortality, among other problems (IPCC, 2014).

Given the aforementioned scenarios, there is a clear need to apply more ambitious goals and to call for a global and integrated vision of the problems, in order to achieve sustainability at a global level.

In September 2015, the 70th United Nations General Assembly took place in New York, in which all Member States of the United Nations (UN) approved the 2030 Agenda for Sustainable Development (UN, 2021b). This Agenda intends to act in the three dimensions of sustainable development (economic, social, and environmental) in an incorporated form

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(UN, 2015). The 2030 Agenda includes 17 Sustainable Development Goals (SDG), associated with 169 targets, which aim to act on urgent global challenges, moving efforts to make the world a safer, fairer, and sustainable place for all (Filho et al., 2019; UN, 2015). In addition to continuing the work developed within the scope of the Millennium Development Goals, the SDGs are now involving all countries and not just the developing countries as before (UNSDSN, 2015). As in the case of Millennium Development Goals, the SDGs also have a 15- year time horizon (República Portuguesa, 2017).

In addition to this, other actions aim to contribute for these changes through a broader vision, acting on several pillars (economy, environment, health, among others) instead of on only one.

In 2014, around 30 countries and several international organizations established the Global Health Security Agenda (GHSA), which aims to act on the infectious diseases that make the world a less safe and healthy place (GHSA, 2018). To encourage this goal, a set of 11 targets were defined, called “Action Packages” (CDC, 2021). Currently, about 70 countries are part of this agenda, as well as several international organizations namely the Food and Agriculture Organization of the United Nations (FAO), World Organization for Animal Health (OIE), World Bank, and the World Health Organization (WHO) (GHSA, 2021). It is important to emphasise that some of the Action Packages act according to the One Health vision. “One Health” corresponds to an approach that encompasses the involvement and cooperation of various sectors (human health, animal health, and the environment) through research and implementation of new measures, with the purposes of achieving optimal results at the level of health (CDC, 2021; WHO, 2021a). This is not a new concept; however, it has gained some prominence in recent years, mainly due to changes in the interactions occurring between living beings and the environment. These interactions include the population growth and consequent geographic expansion that can lead to greater proximity to animals and their habitat; changes in land use (as a consequence of deforestation and intensive agricultural practice) that can provide favourable conditions for the transmission of diseases to animals; and lastly, the more frequent international transport of people, animals, and products that provides faster transmission of diseases (CDC, 2021).

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The economy, environment, and public health are independent but somehow connected sectors, and this perception can be fundamental for embracing measures that, through synergies, are able to translate into a better world for future generations. Therefore, the use of integrated approaches, which comprise the different sectors, can be more advantageous to the goal of achieving a more sustainable world (Galvani, 2016).

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2. State of the art

2.1 Nutrition on human health

Nutrition plays a fundamental role in promoting human health. Consequently, a poorly controlled diet (with small emphasis on fruits, vegetables, nuts and grains, and focused on processed and red meats) is associated with the development of numerous diseases, representing the biggest health problem in the world (Esposito et al., 2017; Springmann et al.

2018). According to Clark (2019), in addition to a poor diet being responsible for most of the top 15 risk factors for morbidity worldwide, diseases associated with this type of diet (e.g., type II diabetes, stroke, and some types of cancers) are also responsible for almost 40% of global mortality.

The maintenance of a healthy diet aims to ensure that all nutrient needs are met, and this depends on different factors such as gender and age (FAO et al. 2020). For adults to reach a healthy diet, the World Health Organization (WHO, 2020) makes several recommendations, which include the incorporation of fruit, vegetables, legumes, nuts and grains; an intake of free sugars that do not exceed 10% of the total energy intake; a consumption of fats under 30% of the total energy intake; and a consumption of less than 5 g of salt per day.

It should be noted that even though a balanced and healthy diet can be achieved, this can be difficult to accomplish because of social and economic issues (WHO, 2020).

According to FAO et al. (2020), it is estimated that more than 3 billion people are not able to economically achieve a healthy diet and that more than 1.5 billion cannot even afford a diet that at least responds to the expectable nutritional needs. In order to mitigate this problem, the governments have a great responsibility, as it is their responsibility to provide the population with the conditions necessary to maintain a healthy diet (WHO, 2021b).

2.2 Impact of diet trends on the environment

According to FAO (2018), a Food System (FS) is defined as “the entire range of actors and their interlinked value-adding activities involved in the production, aggregation, processing, distribution, consumption and disposal of food products that originate from

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agriculture, forestry or fisheries, and parts of the broader economic, societal and natural environments in which they are embedded”. For a food system to be considered sustainable, and according to the same organization (FAO, 2018), it is necessary that this system

“delivers food security and nutrition for all in such a way that the economic, social, and environmental bases to generate food security and nutrition for future generations are not compromised”.

One of the main reasons that compromises the sustainability of the current food system emerges from the growth of the world population – which currently exceeds 7.7 billion people and is expected to reach 10 billion by 2050 – as well as the food trends that are emerging in response to this growth (Fasolin, 2019; Heller et al. 2013; Willett et al. 2019).

In addition to the existing food system being not sustainable, both food production and consumption account for two of the primary environmental degradation causes (Meybeck &

Gitz, 2017). If on one hand, population growth is a high contributor to the demand for agricultural products (FAO, 2017), this growth also means that the availability of suitable land for agriculture is also decreasing (Attwood et al., 2017). To respond to this growth, it is necessary to adopt new approaches that allow a greater production per unit of land (Attwood et al., 2017). To make this possible, processes such as the increased use of chemical fertilizers, pesticides, irrigation, and mechanization are commonly used (Matson et al., 1997). It is currently known that this agricultural intensification can be at the base of several negative consequences such as reduced soil fertility, reduced biodiversity, groundwater pollution, eutrophication of lakes and rivers, or even at the level of atmospheric composition (Matson et al., 1997). Between 2007 and 2016, for example, it was found that the food system was responsible for 21 to 37% of the total greenhouse gases (GHG) emissions, and from these 9 to 14% were derived from agriculture (Mbow et al., 2019). In addition to this, agriculture is also responsible for 70% of the use of freshwater and 50% of the use of habitable land, with livestock production being a high contributor to these percentages (Aleksandrowicz et al., 2016; Mbow, et al. 2019; FAO, 2020; Steinfel et al., 2006).

According to Cucurachi et al. (2019), if the current methods of food production and the current type of consumption are maintained, the perspective is that the impacts of food systems will become increasingly greater. Therefore, it becomes urgent to adopt food

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production strategies capable of responding to the needs generated by the continuous growth of the world population, and respecting the planetary boundaries.

2.3 Seaweeds as a solution for the sustainability of the food system

Seaweeds, otherwise known as marine macroalgae, are macroscopic eukaryotic photosynthetic organisms, mostly benthic (Bykova et al., 2020). Due to its colour, three main groups of seaweeds can be distinguished: Chlorophyta (green algae), Rhodophyta (red algae), and Ochrophyta – Phaeophyceae (brown algae) (Leandro et al., 2020).

Seaweeds play an important role in promoting biodiversity and the proper functioning of marine ecosystems, namely through the provision of services such as shelter, habitat, nursery grounds, and food (Barbier et al., 2019; Prathep et al., 2011; Smale et al. 2013;

Steneck et al., 2002). Another great potential of seaweeds is related to their role in mitigating and adapting to the impacts of climate change. For example, seaweeds have a strong potential for removing CO² from the atmosphere, being this gas one of the most relevant in terms of anthropogenic GHG emissions (Moreira & Pires, 2016). In addition, some seaweeds can play an important role in coastal protection, such as Kelp forests, dampening the impact of waves generated by storms (Lovas and Tørum, 2001).

At present, there are many applications for the seaweeds around the world, including in pharmaceutical and cosmetic industry, fertilizers, chemicals, and food (Pereira, 2011; Soares et al. 2017).

Seaweed production has been growing considerably, and between 2000 and 2018, its volume exceeded threefold, reaching 32.4 million tons (FAO, 2020). In 2019, approximately 35.8 million tons of seaweeds were produced worldwide, reinforcing the growth scenario for this product (Cai et al., 2021). Of the total amount of seaweed produced worldwide, it is worth highlighting the role of Asian countries over the years, and in 2019, these countries were responsible for about 97% of world production (European Commission, 2019; Cai et al., 2021).

Industrially, macroalgae can be obtained in three different ways (Sudhakar et al., 2018):

collecting species from the sea; through collection of seaweeds that come ashore; and

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through cultivation of species. The first two methods are categorized as wild harvesting, while the last one is typically named as aquaculture (Nayar & Bott, 2014). Regarding the last method, the need to resort to seaweed cultivation arises as a consequence of the growth in demand for this product, which in turn leads to an increase in the overexploitation of certain species (Chopin, 2009). Aquaculture stands out in the algae industry, representing in 2019 about 97% of the world's production (Cai et al., 2021).

Figures 1 and 2 represent the worldwide distribution of macroalgae production through aquaculture and wild harvesting, respectively, and were based on the “Brief on algae biomass production”, developed by the European Commission (2019). Through these figures, it is possible to observe that, regarding production through aquaculture, Asian countries stand out with more than 99% of this production. However, the same does not verify for wild harvesting, with the highest portion belonging to Chile. According to the mentioned document, it is noteworthy that between 2014 and 2016, the European Union and Norway, together, contributed only with 0.002% to global production through aquaculture.

It is also mentioned in the same document that, concerning wild harvesting production, the values are higher for the same area, with a contribution of 18% of the global total.

Figure 1 - Global production of macroalgae based on aquaculture (adapted from European Commission, 2019).

China 51,23%

Indonesia 35,40%

Philippines 4,95%

South Korea 3,97%

North Korea 1,67%

Japan 1,28%

Malaysia

0,79% Tanzania

0,49%

Madagascar 0,04%

Chile

0,04% Viet Nam 0,04%

Solomom Islands 0,04%

Other countries 0,04%

Papua New Guinea

0,01%

Kiribati 0,01%

Other 0,72%

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Figure 2 - Global wild harvesting of macroalgae (adapted from European Commission, 2019).

Regarding wild harvesting, the collection of seaweeds can be done mechanically (using vessels with the appropriate equipment) or manually. When done manually, it is relevant to pay attention to the cut location, so that, when done correctly, the seaweed can grow again (Mesnildrey et al., 2012). Regarding seaweed collection using a vessel, there are several techniques that can be performed, which may depend on the species to be collected. One of the frequently mentioned techniques uses a device called "scoubidou" (McHugh, 2003;

Mesnildrey et al., 2012; Monagail et al. 2017; Scottish Government 2016). This device consists of a swivelling iron hook, suspended by a hydraulic arm, which is taken to the algae bed and turns over a mechanism, rolling and pulling the seaweeds (McHugh, 2003; Mesnildrey et al., 2012).

The aquaculture of seaweed can be performed through various techniques (García-Poza et al., 2020): land-based/onshore (using for example, ponds, raceway systems, or tanks);

offshore (where the seaweeds grow in a structure located at sea, away from the coast); or near-shore (when cultivation is developed in estuaries or close to the coast). Among the methods used in these seaweed culture techniques, two can be highlighted (Valderrama et al., 2015): off-bottom systems (Figure 3) and floating systems (Figure 4). The off-bottom technique consists of using a rope with the extremities attached between two structures (stakes or buoys, for example) (McHugh, 2003; Taelman et al., 2015). These structures are

Chile 32,50%

China 21,96%

Norway 14,02%

Japan 7,95%

Indonesia 4,73% France

3,93% Ireland 2,68%

Peru 2,32%

India 1,70%

Iceland 1,61%

Canada 1,16%

Mexico 0,98%

South Africa 0,89%

Russian Federation

0,80%

South Korea 0,80%

Other countries

0,80% United

States … Marroco 0,45%

Spain 0,27%

Other 5,45%

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stabilized (through the use of weights, or buried in the substrate), and the seaweeds grow attached to the rope between these structures (McHugh, 2003; Taelman et al., 2015;

Valderrama et al., 2015). This technique is generally used in the near-shore cultivation method (FAO, 2013a). The floating system employs a floating structure (which can be composed of different materials like bamboo or plastic), where the seaweeds grow suspended from the platform (FAO, 2013a; Taelman et al., 2015; Valderrama et al., 2015).

This structure is attached to the seabed using materials such as ropes and weights (Robledo et al., 2013; Taelman et al., 2015).

Figure 3 - Example of a structure based on the off-bottom technique (Source: Robledo et al., 2013).

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Figure 4 - Example of a structure based on the floating system technique (Source: Robledo et al., 2013).

The use of different techniques in the production of seaweeds leads to different impacts resulting from this activity, also allowing that some techniques reveal to be more advantageous over others.

One of the advantages of seaweed production through land-based aquaculture is the possibility of greater control of the farm, and therefore an adjustment to the most favourable conditions for it, namely in terms of nutrient input, pH, salinity, and light (García-Poza et al., 2020). The fact that this type of aquaculture allows adjustments, gives the possibility of producing a greater range of algae genera, compared to offshore aquaculture, which reveals to be a strong advantage (Hafting et al. 2012). The disadvantages related with land-based aquaculture are mainly the costs associated with the necessary infrastructure, as well as energy expenditure (Hafting et al. 2012; García-Poza et al. 2020). Other less favourable point associated with this production method concerns the need of an area for these large infrastructures, which is not always available or at affordable prices (Hafting et al. 2012;

García-Poza et al. 2020).

Compared to land-based aquaculture, production of seaweeds through offshore aquaculture requires less labour and lower costs associated with infrastructure, which represents a great advantage over the former (Werner & Dring, 2011). In addition, offshore aquaculture has the advantage of not having much competition for space at sea (Roberts &

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Upham, 2012). Although this method does not require the onshore space associated with the seaweed development, like in land-based aquaculture, there is a need to resort to appropriate facilities for the initial stages of algae growth (Nursery phase). This type of space allows the manipulation of certain aspects, namely light and temperature, to optimize the development of seaweeds (Werner & Dring 2011). Another disadvantage of offshore aquaculture is the susceptibility of structures and seaweeds to less favourable environmental conditions in the ocean (García-Poza et al., 2020). Campbell highlights in a 2019 study several consequences associated with the cultivation of seaweeds: For example, the introduction of seaweeds through a suspended method may be responsible for altering the ecosystem's nutrient cycle. This event can be beneficial in terms of remediation of the ecosystem, but it can become unfavourable when the absorption of nutrients by seaweeds prevents the existence of the necessary quantities for the primary producers already existing in the area. This form of seaweed production can also affect the local hydrodynamic movements. Another negative aspect identified by the author involves the fact that this method leads to a greater movement of boats to and from the platform, which consequently may imply the disturbance of certain species due to noise.

In near-shore aquaculture, according to García-Poza et al. (2020), the infrastructure is located close to the coast, meaning that it is less prone to effects caused by sea storms and currents, representing a significant advantage. Near-shore aquaculture also represents an important environmental advantage once it facilitates the bioremediation of river basins polluted due to nutrients coming from the agriculture practiced in the surroundings (García- Poza et al., 2020). In terms of disadvantages, it should be noted that there is a limitation regarding the acquisition of a location to implement this method, since areas along the coast are sought after by sectors such as tourism and urbanism (FAO, 2013).

With the collected bibliography, no great environmental advantages associated with the wild harvesting production method were verified, being its impacts one of the main reasons for the popularity of the cultivation methods. A significant advantage of the wild harvest is associated with its social component. According to Monagail et al. (2017), the wild harvesting of seaweeds is a prominent component in the tradition of many countries. The same authors claim that this is an activity practiced in a family environment and that its

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proceeding operations are generally developed at home or near. Another positive aspect found regarding seaweeds harvesting is the significant participation of women in this activity (Monagail et al., 2017; Marinho-Soriano, 2016). This dominance is essentially due to their knowledge of the coastal environment, which passes through the family generations (Marinho-Soriano, 2016). In terms of the disadvantages of the harvest method, it is important to mention the environmental impacts that can be associated with this method.

When carried out on a large scale, this type of harvest can affect the ecosystem services offered by the algae, particularly habitat, shelter, nursery, coastal protection, and carbon sequestration (Scottish Government, 2016). Exhaustive removal of seaweed can also interfere with the local availability of some resources, namely light and space (Vasquez, 1995). These consequences naturally depend on several factors, such as location, the species in question, or the amount collected (Scottish Government, 2016). In addition to the environmental consequences caused by harvesting seaweeds, there are other cons associated with this method. Natural phenomena such as the height of waves, currents, and weather, can affect the harvest, representing a consequence for production. (Monagail et al., 2017).

In general, a consequence that may arise from seaweed production in the natural aquatic environment is the abandonment of certain materials used in this activity, namely stakes, ropes, and floats (FAO, 2013a; Neish, 2008). Another effect of this production is related with invasive species. According to Lockwood et al. (2013), invasive species are those that evolved in a given location and that, by some means, were introduced in another area, in which they established and spread, causing damage to the new environment (as cited in James, 2016). Once established, these species compete with native species and generally have advantages such as high reproductive rates and the existence of few predators in the new area (Máximo et al, 2018). When the entry of a non-native species occurs in a certain environment, its elimination becomes quite difficult (Campbell et al., 2019). These species can represent inconvenient changes in the surrounding environment, affecting the structure and function of ecosystems (Bulleri et al., 2012). Regarding the cause of the introduction of these species in the new receiving environment, this may occur accidentally (for example, through imported organisms, movement of aquaculture equipment, attached to the hull of ships, or equipment from vessels such as anchors, ropes, and floats) or deliberately through

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aquaculture, being this the main vector of introduction of these species (James & Shears, 2016; Sinner et al., 2020; Naylor et al., 2001; Petrocelli & Cecere, 2015).

The following table (Table 1) summarizes the mentioned pros and cons, associated with each of the four described methods aquaculture land-based, offshore and near-shore and wild harvest.

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Table 1- Identified pros and cons, associated with the four types of seaweed production.

Seaweed aquaculture Wild Harvest

Land-based Offshore Near-shore

Pros

Control and monitoring of the environmental conditions for

seaweed production

More economical compared to land-based

Protected by the land from sea

agitation Reduced land use

Allows the production of more algae genera

Less labour compared to land- based

Facilitation of bioremediation of

river basins Tradition for many countries

- No competition for space at sea - Inclusion of women in work

Cons

Land use availability/competition

Susceptibility of infrastructure to adverse

conditions

Competition between sectors Loss of associated ecosystem services Costs associated with high energy

consumption

Increased movement of boats and the consequent disturbance of

some species

Change in nutrient cycle and hydrodynamic movements

Production depends on factors such as weather Costs associated with

infrastructure Introduction of invasive species Abandonment of material inherent to seaweed production

Abandonment of material inherent to seaweed production.

- Change in nutrient cycle and

hydrodynamic movements - -

- Abandonment of material inherent

to seaweed production - -

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Regarding its use as human food, currently more than 600 species of edible algae are known (Leandro et al., 2020). Among the species with commercial value, those that correspond to the highest production are Kappaphycus alvarezii, Eucheuma denticulatum, Gracilaria verrucosa, Saccharina japonica, Porphyra spp. and Undaria pinnatifida (the last three being generally known as Kombu, Nori and Wakame, respectively) (WBG, 2016). The evolution of the production of these species through aquaculture is shown in Figure 5. It should be noted that, for Gracilaria verrucosa, no data was found regarding evolution of production for this species. Therefore, for this figure, the data of all genera Gracilaria was considered.

Figure 5 - Production evolution of Kappaphycus alvarezii, Eucheuma denticulatum, Gracilaria verrucosa, Saccharina japonica, Porphyra spp., and Undaria pinnatifida over the years.

The incorporation of seaweed in the human diet is not a novelty, especially for Asian countries such as China, Japan, and Korea, being currently one of the most used foods (Cotas et al., 2021; Leandro et al., 2020; McHugh, 2003). Regarding Europe, the situation is different, because as in addition to its consumption having started later, there is also no frequent use for this food in these countries’ diet (Wendin & Undeland, 2020). Despite this, some studies report the existence of a growing interest on the part of consumers in several European countries (Palmieri et al., 2020).

6906,2

11230,1

12871,4

19421,0 20026,4 21162,5 21013,5

0 5000 10000 15000 20000 25000

2000 2005 2010 2015 2016 2017 2018

Thousand tonnes (live weight)

Year

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There is an interesting nutritional value associated with algae, as they are considered good sources of vitamins, minerals, protein and dietary fiber, as well as being low in calories (Koru et al., 2013; Pereira, 2010; Pereira, 2011; Wendin, 2020). Iodine, for instance, is an element found in satisfactory amounts in seaweeds, which contributes to the proper functioning of the thyroid gland (Pereira, 2010). Therefore, the incorporation of seaweed in the diet may prove to be beneficial, not only because of its ability to attend to possible dietary deficits, but also to prevent disorders such as cardiovascular and cerebrovascular disease, and cancer (Cotas et al., 2021; Thawadi, 2018).

Despite the health benefits associated with seaweeds, there may be some hesitation towards its introduction in the human diet, since these organisms can accumulate harmful substances (Cotas, 2021). This is the case for heavy metals such as arsenic, lead, cadmium, and mercury (Cotas, 2021; Monteiro et al., 2019). Iodine also requires some attention since, as mentioned above, it is found in large amounts in seaweeds (especially in brown algae), and a high exposure can result in problems such as dysfunction of the thyroid gland (Holdt &

Kraan, 2011; Monteiro et al., 2019). It should also be noted that, apart from depending on the species, the composition of algae can also differ according to the season, geographic location or even the temperature of the water (Koru et al., 2013; MacArtain et al., 2007).

As previously stated, seaweeds can positively impact the human health.

Furthermore, these organisms may present themselves as a sustainable food resource, which is related to its presence in almost all ecosystems and its fast growth (Nova et al., 2020).

2.4 Regulation

As seen above, high exposure to some contaminants such as lead, mercury, cadmium, and arsenic, or even to certain nutrients such as iodine, can prove to be dangerous (National Food Institute et al., 2019), so control and recommendations regarding its intake become paramount. However, since algae do not represent great importance in the human diet in most European countries, there are still few European Union (EU) regulations concerning the use of this product as food (Lähteenmäki-Uutela et al., 2021).

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At the European level, in December 2006, the Regulation (EC) No. 1881/2006 sets the maximum levels (ML) for certain contaminants in foodstuffs. According to the Commission Recommendation (EU) 2018/464 of 19 March 2018, regarding arsenic, cadmium, and lead, ML for various foodstuffs are established in Regulation (EC) No. 1881/2006, however, these values are not established for these substances in seaweeds. Afterwards, the consolidated version of Regulation (EC) No. 1881/2006 establishes a maximum level of 3.0 mg/kg wet weight for cadmium in food supplements consisting exclusively or mainly of dried seaweed or products derived from seaweed, as well as a maximum of 0.1 mg/kg wet weight and 3.0 mg/kg wet weight for mercury and lead respectively, in food supplements in general.

Although there is not much regulation regarding the consumption of algae, the entry of an algae species or derivative on the market is controlled by Regulation (EC) No 258/97 (Lähteenmäki-Uutela et al., 2021). This regulation, established in 1997, defines that, to protect public health, before being placed on the market, all novel foods and novel food ingredients must undergo a safety assessment. Novel food is considered to be food that has not been consumed to a significant degree by humans before May 15th, 1997 (date of entry into force of the aforementioned regulation) (EC, 2021a). In 2017, the Regulation (EU) 2017/2470 is launched, which establishes the list of novel foods to be authorized on the market, called “The Union List”. Currently the European Commission also has an online list (the Novel Food Catalogue), which contains the various foods on the Union List (Lähteenmäki-Uutela et al., 2021). In this online list, it is possible to find relevant information such as the product description and its regulatory status (EC, 2021b). Therefore, this list presently includes more than 20 species of seaweeds, some of which are used as food (Lähteenmäki-Uutela et al., 2021).

In 2018, the European Union established, through the Commission Recommendation (EU) 2018/464 of 19 March 2018, the recommendation that all Member States accomplish, between 2018 and 2020, the monitoring of the presence of arsenic, cadmium, iodine, lead and mercury in algae, halophytes and products based on seaweed, in partnership with food and feed business operators.

Regarding European countries, France was the first country to define specific regulations regarding the human consumption of seaweed (APN, 2020). The procedure

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adopted by the country in the early 1980s is similar to that of the European Union, also leading to the definition of a list of edible algae (CEVA, 2021). As for Portugal, there is still no regulation at this level, which is also due to the low pressure exerted by the market on these products (Pereira, 2021).

2.5 Seaweeds in Portugal

The Portuguese coast has a range of several characteristics, such as the nutrient regime and the sea surface temperature, which results in a very interesting and diversified algal flora (Gaspar et al., 2019). A curious aspect regarding the algal community present on this coast is that in the north of the country there is a higher amount of brown algae species compared with the red species, whereas in the south there is an opposite trend (APN, 2019;

Pereira, 2010).

In the early 1970’s, Ardré published the result of what was an intensive study of the algal community on the Portuguese coast, reporting the existence of 460 species (Gaspar et al., 2019; Pereira, 2010). However, a more recent study describes the existence of 527 species (Zugasti, 2011). In addition to his contribution to updating the numbers on this checklist, Zugasti (2011) highlights the northward migration of species from the south of the Portuguese coast, which is caused by an increase of the sea surface temperature.

Even though there is a great diversity and abundance of algae along the Portuguese coast, this type of product is not typically consumed in the country’s traditional diet, and its intake only occurs when associated with the consumption of Japanese food (Soares et al., 2017). However, the situation is different in the Azores islands, since there are several populations that integrate macroalgae in their diet (APN, 2019; Pereira, 2010; Soares et al., 2017). Some of the species most used by these populations include Porphyra leucostica, Osmundea pinnatifida and Ulva intestinalis (APN, 2019; Pereira, 2010).

As mentioned above, the Portuguese coast possesses a set of different characteristics that enhance the diversity of algae species. However, despite being an expanding industry, there are currently few national companies dedicated to this product in Portugal (APN, 2019, Pereira 2021). Due to the shortage of agar from Asian countries during World War II, Portugal expanded on this industry, growing into one of the main producers at a global

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level in the 1970’s (Leite, 2017; Pereira, 2010). However, several factors namely the overexploitation of some algae species used in the production of agar and their consequent disappearance caused a decline in this industry, with only one operational factory currently existing in the country (Leite, 2017; Pereira, 2010). In response to this risk associated with overexploitation, there has been an improvement of the techniques used in algae cultures (Pereira, 2010).

Regarding the production of algae through aquaculture, the number of companies responsible for this activity is still diminished. The company Algaplus, founded in 2012, stands out in the sustainable cultivation of indigenous macroalgae from the Atlantic coast, with the purpose of generating food and cosmetic products (Algaplus, 2021a). The company has an annual production of 40 tons, of which 75% is exported (Algaplus, 2021b). More recently, the company Aquazor - Aquaculture and Marine Biotechnology of the Azores launched a new project which aims to study the potential production of algae and fish in offshore aquaculture (Portugal2020, 2019; RTP Açores, 2020).

Even though there is still some reluctance by the Portuguese trade about the seaweeds, research continues and is being reinforced in order to increase the knowledge about Portuguese seaweeds (Gaspar et al., 2019; Pereira, 2021). This study is motivated by the potential of the seaweeds as a food product for the population and intents to change the paradigm around the integration of this product in the Portuguese diet (Pereira, 2021; Soares et al., 2017).

2.6 Risk-benefit assessment

Despite being essential for human life and responsible for great health benefits, foods may also have some associated risks. This can be due to the potential presence of natural toxins, dangerous chemicals and pathogenic organisms, and also result from an unbalanced nutrient intake, i.e., in doses higher or lower than those necessary for humans (Nauta et al.

2018; Verhagen et al. 2021).

According with the Guidance on human health risk-benefit assessment of foods developed by EFSA Scientific Committee (2010), risk is defined as the probability of an adverse effect occurring as a result of exposure to a particular agent, while benefit is the probability of a

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positive health effect. It should be noted that, according to the same guidance, the reduction of a risk also represents a benefit.

The assessment of risks and benefits began as independent studies serving distinct purposes and to which different methodologies were applied (Fransen et al., 2010; Tijhuis et al., 2012). However, this separate approach proves to be insufficient from the point of view of food authorities, leading to the need for a combined assessment to understand the balance between the risks and benefits of a particular food or food component, as well as the net health impact (Hart et al., 2013; Thomsen, 2018). This modification led to the development of the risk-benefit assessment (RBA). Tijhuis et al. (2012), describes RBA as the scientific process to estimate the risks and benefits to humans that result from exposure (or lack of) to a particular food/food component. The RBA should also represent a support tool for policymakers in order to develop strategies that contribute to a healthy diet (Thomsen, 2018;

Verhagen et al., 2021).

The suggested procedure by EFSA Scientific Committee to perform the risk-benefit assessment is mainly based on the process used for the risk assessment, and comprises the following steps: identification and characterisation of adverse effects, exposure assessment and risk characterisation (EFSA Scientific Committee, 2010; Thomsen, 2018; Tijhuis et al., 2012). In parallel, for the benefit assessment, the following steps are applied: identification and characterization of beneficial effects, exposure assessment and benefit characterization (EFSA Scientific Committee, 2010; Thomsen, 2018). Exposure assessment is a common step for both the risk and the benefit elements of the process and accounts for relevant dietary and non-dietary sources (EFSA Scientific Committee, 2010). The two arms finally converge in the last step (risk-benefit comparison) where the balance between risks and benefits is done through a common measure to assess the net impact on health (EFSA Scientific Committee, 2010; Thomsen, 2018). In Figure 1 the paradigm for the risk-benefit assessment recommended by the Scientific Committee of EFSA is presented.

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2.7 Seaweeds and its contribution to Sustainable Development Goals

Through the information collected and mentioned until this subchapter, it is possible to verify the potential of seaweeds consumption and production for many of the Sustainable Development Goals. For example, as previously stated, seaweeds prove to be good sources of vitamins, minerals, among other nutrients. The presence of these nutrients in this type of food reveals its potential as a contributor to the achievement of Goal 2 – Zero hunger. The seaweeds’ ability to remove CO² from the atmosphere, as well as its importance in coastal protection, are two ecosystem services that greatly contribute to the fulfilment of the 13^th Goal - Climate Action. It is also important to highlight the integration of female workers in the seaweeds production, an aspect that can make a strong contribution to the achievement of Goal 5 - Gender equality.

Several studies assess this relationship between activities associated with macroalgae production and its consumption, with the potential contribution to achieving SDGs. In a study developed by Hossain et al. (2021), whose objective was to understand the role of seaweeds production concerning SDGs and the blue economy in Bangladesh, the

Figure 6 - Risk-benefit assessment paradigm. Adapted from EFSA (2010) and Thomsen (2018).

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importance of seaweed farming in 8 of the 17 Sustainable Development Goals is suggested, more specifically in 26 targets.

In a 2019 study, Bohlin sought to analyse the applicability and usefulness of assessing the sustainability of an emerging industry, based on the SDGs, using the algae industry as a case study. Based on the bibliography, the author associated the various impacts of the seaweed industry to the several targets of Sustainable Development Goals, focusing on those with the greatest relevance. This study allowed the connection with 7 of the 17 Sustainable Development Goals, more specifically with 13 of 169 targets.

With the information present in these studies, it was found that the production and inclusion of seaweeds in the human diet can contribute at least with 11 of the 17 SDGs, and 31 targets. The table below (Table 2) presents several characteristics associated with the production and consumption of seaweeds identified by the authors as favourable aspects for achieving specific targets.

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Table 2 - Actions resulting from the production and consumption of seaweeds, and respective potential goals and targets to be achieved as a consequence of these activities.

Main arguments used Author Goal Target

Seaweed production through a multitrophic production system

Hossain et al.

(2021)

2 - End hunger, achieve food security and improved

nutrition and promote sustainable agriculture 17 - Strengthen the means

of implementation and revitalize the Global Partnership for Sustainable

Development

2.1 - By 2030, end hunger and ensure access by all people, in particular the poor and people in vulnerable situations, including

infants, to safe, nutritious and sufficient food all year round 2.2 - By 2030, end all forms of malnutrition, including achieving, by

2025, the internationally agreed targets on stunting and wasting in children under 5 years of age, and address the nutritional needs of adolescent girls, pregnant and lactating women and older persons

17.7 Promote the development, transfer, dissemination and diffusion of environmentally sound technologies to developing

countries on favourable terms, including on concessional and preferential terms, as mutually agreed

Investing in eco-friendly seaweed production could allow the most vulnerable people to access resources, create decent jobs for both

men and women, as well as guarantee the participation of women in food production.

Furthermore, it could contribute to local economic growth and also increase the resilience of the poorest coastal communities

Hossain et al.

(2021)

1 - End poverty in all its forms everywhere 5 - Achieve gender equality

and empower all women and girls

8 - Promote sustained, inclusive and sustainable economic growth, full and

productive employment and decent work for all

1.4 - By 2030, ensure that all men and women, in particular the poor and the vulnerable, have equal rights to economic resources, as well

as access to basic services, ownership and control over land and other forms of property, inheritance, natural resources, appropriate

new technology and financial services, including microfinance 1.5 - By 2030, build the resilience of the poor and those in vulnerable situations and reduce their exposure and vulnerability

to climate-related extreme events and other economic, social and environmental shocks and disasters

5.1 - End all forms of discrimination against all women and girls

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Main arguments used Author Goal Target everywhere

5.5 - Ensure women’s full and effective participation and equal opportunities for leadership at all levels of decision making in

political, economic and public life

8.1 - Sustain per capita economic growth in accordance with national circumstances and, in particular, at least 7 per cent gross

domestic product growth per annum in the least developed countries

8.2 - Achieve higher levels of economic productivity through diversification, technological upgrading and innovation, including

through a focus on high-value added and labour-intensive sectors 8.3 - Promote development-oriented policies that support productive activities, decent job creation, entrepreneurship, creativity and innovation, and encourage the formalization and growth of micro-, small- and medium-sized enterprises, including

through access to financial services

8.5 - By 2030, achieve full and productive employment and decent work for all women and men, including for young people and persons with disabilities, and equal pay for work of equal value Seaweed cultivation can play an important

role in efficiently promoting marine natural resources. Furthermore, it can help combat

Hossain et al.

(2021)

12 - Ensure sustainable consumption and production patterns

12.2 - By 2030, achieve the sustainable management and efficient use of natural resources

Seaweeds in the human diet as an alternative to achieve the Sustainable Development Goals: A risk-benefit approach

Seaweeds in the human diet as an alternative to achieve the Sustainable Development Goals: A risk-benefit

approach

Maria Beatriz Marta Ferreira de Jesus Fernandes

DEPARTAMENTO DE CIÊNCIAS E ENGENHARIA DO AMBIENTE

MESTRADO INTEGRADO EM ENGENHARIA DO AMBIENTE - Perfil de Engenharia de Sistemas Ambientais

Universidade NOVA de Lisboa

Licenciada em Ciências de Engenharia do Ambiente

DEPARTAMENTO DE CIÊNCIAS E ENGENHARIA DO AMBIENTE

Seaweeds in the human diet as an alternative to achieve the Sustainable Development Goals: A risk- benefit approach

Maria Beatriz Marta Ferreira de Jesus Fernandes Licenciada em Ciências de Engenharia do Ambiente

ACKNOWLEDGMENTS

ABSTRACT

RESUMO

LIST OF ABBREVIATIONS

TABLE OF CONTENTS

LIST OF FIGURES

LIST OF TABLES

1. Introduction

2. State of the art

2.1 Nutrition on human health

2.2 Impact of diet trends on the environment

2.3 Seaweeds as a solution for the sustainability of the food system

2.4 Regulation

2.5 Seaweeds in Portugal

2.6 Risk-benefit assessment

2.7 Seaweeds and its contribution to Sustainable Development Goals