The green seaweed Ulva: tomorrow’s “wheat of the sea” in foods, feeds, nutrition, and biomaterials
Abstract
Ulva, a genus of green macroalgae commonly known as sea lettuce, has long been recognized for its nutritional benefits for food and feed. As the demand for sustainable food and feed sources continues to grow, so does the interest in alternative, plant-based protein sources. With its abundance along coastal waters and high protein content, Ulva spp. have emerged as promising candidates. While the use of Ulva in food and feed has its challenges, the utilization of Ulva in other industries, including in biomaterials, biostimulants, and biorefineries, has been growing. This review aims to provide a comprehensive overview of the current status, challenges and opportunities associated with using Ulva in food, feed, and beyond. Drawing on the expertise of leading researchers and industry professionals, it explores the latest knowledge on Ulva’s nutritional value, processing methods, and potential benefits for human nutrition, aquaculture feeds, terrestrial feeds, biomaterials, biostimulants and biorefineries. In addition, it examines the economic feasibility of incorporating Ulva into aquafeed. Through its comprehensive and insightful analysis, including a critical review of the challenges and future research needs, this review will be a valuable resource for anyone interested in sustainable aquaculture and Ulva’s role in food, feed, biomaterials, biostimulants and beyond.
Full text
Critical Reviews in Food Science and Nutrition ISSN: (Print) (Online) Journal homepage: www.tandfonline.com/journals/bfsn20 The green seaweed Ulva: tomorrow’s “wheat of the sea” in foods, feeds, nutrition, and biomaterials Laurie C. Hofmann, Sylvia Strauss, Muki Shpigel, Lior Guttman, Dagmar B. Stengel, Céline Rebours, Natasha Gjorgovska, Gamze Turan, Karina Balina, Gabrielle Zammit, Jessica M. M. Adams, Umair Ahsan, Angela G. Bartolo, John J. Bolton, Rosário Domingues, Ömerhan Dürrani, Orhan Tufan Eroldogan, Andreia Freitas, Alexander Golberg, Kira I. Kremer, Francisca Marques, Massimo Milia, Sophie Steinhagen, Ekin Sucu, Liliana Vargas- Murga, Shiri Zemah-Shamir, Ziv Zemah-Shamir & Antonio J. Meléndez- Martínez To cite this article: Laurie C. Hofmann, Sylvia Strauss, Muki Shpigel, Lior Guttman, Dagmar B. Stengel, Céline Rebours, Natasha Gjorgovska, Gamze Turan, Karina Balina, Gabrielle Zammit, Jessica M. M. Adams, Umair Ahsan, Angela G. Bartolo, John J. Bolton, Rosário Domingues, Ömerhan Dürrani, Orhan Tufan Eroldogan, Andreia Freitas, Alexander Golberg, Kira I. Kremer, Francisca Marques, Massimo Milia, Sophie Steinhagen, Ekin Sucu, Liliana Vargas-Murga, Shiri Zemah-Shamir, Ziv Zemah-Shamir & Antonio J. Meléndez-Martínez (09 Jul 2024): The green seaweed Ulva: tomorrow’s “wheat of the sea” in foods, feeds, nutrition, and biomaterials, Critical Reviews in Food Science and Nutrition, DOI: 10.1080/10408398.2024.2370489 To link to this article: https://doi.org/10.1080/10408398.2024.2370489 © 2024 The Author(s). Published with license by Taylor & Francis Group, LLC. View supplementary material Published online: 09 Jul 2024. Submit your article to this journal Article views: 2850 View related articles
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CritiCal reviews in Food sCienCe and nutrition The green seaweed Ulva: tomorrow’s “wheat of the sea” in foods, feeds, nutrition, and biomaterials Laurie C. Hofmanna,b, Sylvia Straussc, Muki Shpigeld, Lior Guttmane,f, Dagmar B. Stengelg, Céline Reboursh, Natasha Gjorgovskai, Gamze Turanj, Karina Balinak,l, Gabrielle Zammitm, Jessica M. M. Adamsn, Umair Ahsano,p, Angela G. Bartoloq, John J. Boltonr, Rosário Dominguess,t, Ömerhan Dürraniu, Orhan Tufan Eroldoganv,w, Andreia Freitasx,y, Alexander Golbergz, Kira I. Kremer, Francisca Marquess,t, Massimo Miliaab, Sophie Steinhagenac, Ekin Sucuad, Liliana Vargas-Murgaae, Shiri Zemah-Shamiraf, Ziv Zemah-Shamirag and Antonio J. Meléndez-Martínezah* aalfred wegener institute, Helmholtz Center for Polar and Marine research, Bremerhaven, Germany; bBremerhaven university of applied sciences, Bremerhaven, Germany; cthe seaweed Company, schiedam, the netherlands; dMorris Kahn Marine research station, the leon H. Charney school of Marine sciences, university of Haifa, Haifa, israel; ethe national Center for Mariculture, israel oceanographic & limnological research, eilat, israel; fdepartment of life sciences, Ben-Gurion university of the negev, Beer-sheva, israel; gBotany and Plant science, school of natural sciences, university of Galway, Galway, ireland; hMøreforsking as, Ålesund, norway; iinstitute of animal science and Fishery, university ss Ciril and Methodius in skopje, skopje, north Macedonia; jaquaculture department, Fisheries Faculty, ege university, Bornova, izmir, türkiye; kinstitute of Microbiology and Biotechnology, university of latvia, riga, latvia; linstitute of science and innovative technologies, liepaja university, liepaja, latvia; mdepartment of Biology, Faculty of science, university of Malta, Msida, Malta; ninstitute of Biological, environmental and rural sciences (iBers), aberystwyth university, aberystwyth, uK; odepartment of Plant and animal Production, Burdur vocational school of Food, agriculture and livestock, Burdur Mehmet akif ersoy university, Burdur, turkiye; pCenter for agriculture, livestock and Food research, Burdur Mehmet akif ersoy university, Burdur, turkiye; qenvironment & resources authority, Marsa, Mrs, Malta; rdepartment of Biological sciences, university of Cape town, rondebosch, south africa; sdepartment of Chemistry, lipidomics laboratory, Mass spectrometry Centre, university of aveiro, santiago university Campus, aveiro, Portugal; tdepartment of Chemistry, CesaM – Centre for environmental and Marine studies, university of aveiro, santiago university Campus, aveiro, Portugal; udepartment of Fisheries technology engineering, Faculty of Marine science, Karadeniz technical university, trabzon, türkiye; vdepartment of aquaculture, Faculty of Fisheries, Cukurova university, adana, türkiye; wBiotechnology research and application Center, Cukurova university, adana, türkiye; xnational institute for agricultural and veterinary research (iniav), rua dos lágidos, lugar da Madalena, vila do Conde, Portugal; yreQuiMte/laQv, r. d. Manuel ii, oporto, Portugal; zdepartment of environmental studies, Faculty of exact sciences, Porter school of environment and earth sciences, tel aviv university, tel aviv, israel; aaMarine Biology, university of Bremen, Bremen, Germany; abdepartment of life and environmental science, university of Cagliari, Cagliari, italy; acdepartment of Marine sciences, tjärnö Marine laboratory, university of Gothenburg, strömstad, sweden; addepartment of animal science, agricultural Faculty, Bursa uludag university, Bursa, turkey; aedepartment of Chemical and agricultural engineering and agrifood technology, Polytechnic school, universitat de Girona, Girona, spain; afschool of sustainability, reichman university (idC Herzliya), Herzliya, israel; agdepartment of Marine Biology, leon H. Charney school of Marine sciences, university of Haifa, Haifa, israel; ahFacultad de Farmacia, Food Colour and Quality laboratory, universidad de sevilla, sevilla, spain ABSTRACT Ulva, a genus of green macroalgae commonly known as sea lettuce, has long been recognized for its nutritional benefits for food and feed. As the demand for sustainable food and feed sources continues to grow, so does the interest in alternative, plant-based protein sources. With its abundance along coastal waters and high protein content, Ulva spp. have emerged as promising candidates. While the use of Ulva in food and feed has its challenges, the utilization of Ulva in other industries, including in biomaterials, biostimulants, and biorefineries, has been growing. This review aims to provide a comprehensive overview of the current status, challenges and opportunities associated with using Ulva in food, feed, and beyond. Drawing on the expertise of leading researchers and industry professionals, it explores the latest knowledge on Ulva’s nutritional value, processing methods, and potential benefits for human nutrition, aquaculture feeds, terrestrial feeds, biomaterials, biostimulants and biorefineries. In addition, it examines the economic feasibility of incorporating Ulva into aquafeed. Through its comprehensive and insightful analysis, including a critical review of the challenges and future research needs, this review will be a valuable resource for anyone interested in sustainable aquaculture and Ulva’s role in food, feed, biomaterials, biostimulants and beyond. © 2024 the author(s). Published with license by taylor & Francis Group, llC. CONTACT laurie C. Hofmann laurie.c[email protected] *senior author supplemental data for this article can be accessed online at https://doi.org/10.1080/10408398.2024.2370489. https://doi.org/10.1080/10408398.2024.2370489 this is an open access article distributed under the terms of the Creative Commons attribution license (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. the terms on which this article has been published allow the posting of the accepted Manuscript in a repository by the author(s) or with their consent. KEYWORDS Ulva; food; feed; aquafeed; nutrition; biomaterials; biorefinery; seaweed REVIEW
2 L. C. HOFMANN ETAL. 1. Introduction The world population is expected to reach 9.8 billion by 2050 (Population Reference Bureau, 2023). Accordingly, the agricultural food gap will increase due to climate change-induced constraints on natural resources, i.e., freshwater and farmland. Consequently, ensuring food security has become a global imperative. The oceans will play an increasingly important role in feeding the growing population with increasing demand for food and natural resources. Nevertheless, wild stocks cannot meet the increasing demand for fish or other biomass sources, including macroalgae. Therefore, seaweed cultivation may be essential for contributing to food security by provisioning food or feed ingredients (Araújo et al. 2022; Forster and Radulovich 2015; Radulovich et al. 2015). Marine macroalgae, commonly known as seaweed, are considered the “promising plant of the millennium” (Dhargalkar and Neelam 2005) because of several advantages over land plants, such as no need for arable land, freshwater, fertilizer or pesticides to grow them, and the biomass can be utilized as food, feed, materials, gelling substances, and biofuels (e.g., Chapman and Chapman 1980). Furthermore, macroalgae grow more rapidly and occupy space more efficiently than terrestrial plants (Creed etal. 2019). In optimal conditions, macroalgae can produce higher dry biomass per unit area per year than fast-growing terrestrial crops such as sugar cane (Gao et al. 1994). Furthermore, macroalgae cultivation may help reduce greenhouse gas emissions in the food system by replacing food, feed, and materials with higher carbon footprints (Troell et al. 2022). Seaweed production and processing can support the blue circular economy by contributing to the key drivers of the circular bio-based economy in the EU (Lange et al. 2021), namely bio-based products for health and new functionalities, primary production, land-use change, sustainable agriculture, biorefineries, and biomass supply for new biorefinery technologies. Further, many recent publications have promoted seaweed cultivation to meet many of the United Nations’ global sustainable development goals (UNSDGs), including reducing hunger, improving good health and well-being, providing affordable and clean energy, and mitigating climate change (Duarte, Bruhn, and Krause-Jensen 2022). Despite these potential contributions to the circular economy, seaweed production in Europe is lagging (Araújo et al. 2021), and many risks and benefits must be assessed before upscaling macroalgal productions into sustainable seaweed aquaculture. These include (i) food safety considerations in integrated multi-trophic aquaculture (IMTA)/waste streams, (ii) genetic interactions of wild crops with cultivated crops, (iii) impacts of seaweed aquaculture on the surrounding ecosystems, (iv) diseases and epiphytes, (v) area utilization from a marine spatial planning perspective, (vi) threats associated with climate change, (vii) using a precautionary approach during carbon accounting and blue carbon financing, (viii) technological advancement for upscaling, and (ix) overcoming legal and economic constraints (Bermejo et al. 2022; Chopin, 2021; Cottier-Cook et al. 2016; Hasselström et al. 2022; Loureiro, Gachon, and Rebours 2015; Rosa etal. 2020, 2019; Stévant, Rebours, and Chapman 2017; Troell et al. 2022). Although algal cultivation technology has improved in the last decade, there is still a need to optimize production for energy efficiency, product quality, consumer safety, and biomass utilization (Stévant, Rebours, and Chapman 2017). Green algae in the genera Ulva, due to the characteristics described below, show high potential for becoming ideal model organisms for innovative mariculture. In the last 30 years, Ulva spp. have been extensively analyzed for their value as food, feed, food ingredients (e.g., protein, carbohydrates, pigments, antioxidants), chemical constituents and medicinal properties, and the number of scientific publications involving Ulva has increased from 2130 in 2000 to 6724 in 2023 (Google Scholar). Major advancements have been made in cultivation methods, molecular identification techniques, and in the fields of aqufeed, terrestrial feed, biostimulants, biomaterials, and biorefinery strategies. From a food and feed perspective, green algae in the genus Ulva contain suitable levels of proteins, vitamins, trace minerals, and dietary fibers (Toth etal. 2020; Trigo et al. 2021; Stedt, Trigo, et al. 2022; Stedt, Toth, et al. 2022; Steinhagen, Larsson, et al. 2022; Steinhagen, Enge, et al. 2021; Steinhagen, Enge, et al. 2022; Taboada, Millán, and MÃguez 2009) for human and animal consumption. The growing world population, environmental awareness and associated increased trends in vegetarianism and veganism, increasing demand for organic products, and global resource shortages are increasing the demand for sustainable marine crops and alternative proteins (Ismail et al. 2020; Faber et al. 2021; Yong et al. 2022; Duarte, Bruhn, and Krause-Jensen 2022). Furthermore, increasing environmental degradation and climate change awareness has actively encouraged health-promoting programs to link human diet and health with environmental sustainability (Patrick and Kingsley 2017). Considering that unhealthy diets primarily cause non-communicable diseases (NCDs), which are a leading cause of death (Lauber et al. 2020), health-promoting foods and lifestyles have attracted the world’s attention. Indeed, the increase in the consumption of plant (and algae)-derived foods is recommended, as they are usually healthier and more sustainable (Willett et al. 2019) protein sources. Nevertheless, the much-cited EAT-Lancet Commission work discussing the need for identifying alternative sustainable food sources in the Anthropocene pays little attention to algae, although aquatic habitats (accounting for 70% of the Earth) will be critical in identifying novel sustainable and health-promoting foods such as seaweed. With an amino acid composition comparable to soy or egg protein, and including all essential amino acids (except tryptophan), selected strains of Ulva bearing high protein contents can partially substitute less sustainable protein sources (Dominguez and Loret 2019), and high contents of essential dietary fiber and other bioactive substances render it a beneficial food item providing health and functional advantages (Rajapakse and Kim 2011; Holdt and Kraan 2011; Lopes etal. 2019; Moreira etal. 2022; Qi etal. 2005). In particular, phytochemicals (e.g., carotenoids, phenolics) have health-benefiting characteristics and can be used in the cosmeceutical and pharmaceutical sectors and as functional
CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 3 foods (Abd El-Baky, El-Baz, and El-Baroty 2009; Khairy and El-Sheikh 2015; Lanfer-Marquez, Barros, and Sinnecker 2005; Mapelli-Brahm et al. 2020; Meléndez-Martínez et al. 2021; Steinhagen, Enge, et al. 2021; Steinhagen, Larsson, et al. 2022; Steinhagen, Enge, et al. 2022), increasing the economic value of Ulva biomass. While Ulva spp., and seaweed in general, remains a niche product in Europe, the European market may play an important role in the future of seaweed production and consumption. Currently, the main importing countries of seaweed in Europe are the UK, France and Germany according to the Center for the Promotion of Imports from developing countries (CBI Ministry of Foreign Affairs). Therefore, the aim of this review is to improve awareness of the seaweed Ulva in food, feed, and beyond and to provide a critical review of the current status, challenges and opportunities of incorporating this genus into the mainstream so that it may become tomorrow’s “wheat of the sea.” To this end, Ulva spp. can play a pivotal role in the sustainable and health-promoting food era, and its consumption and applications are expected to increase in the future. The sustainable exploitation of Ulva as food and feed can contribute to the demand for renewable and novel nutritious food sources, especially with vegetarian and vegan protein, emphasized by the UNSDGs (United Nations, 2015). Because of its valuable constituent composition, Ulva can be biorefined to obtain and valorize products, including food ingredients, materials, chemicals, and fuels, consistent with the new circular economy paradigm. Of course, consumption of seaweeds in general and Ulva in particular also raises safety concerns as it may entail microbiological or chemical risks. This review explores contemporary Ulva research through a comprehensive analysis of their distinct chemical composition, production, uses as food, feed, and biomaterials, and other important aspects, such as nutritional value, food safety, and emerging research needs. This review is targeted toward not only scientists and industry professionals working with seaweed-based foods, feeds and biomaterials, but also food scientists, nutritionists, feed manufacturers, dietitians, cooks, and pharmacists less familiar with Ulva as an ingredient or additive. We provide a critical review of the current status, challenges and future needs that are necessary to bring Ulva and Ulva-based products closer to the forefront of food science and nutrition research. 2. Ulva – tomorrow’s “wheat of the sea” Marine aquaculture is the fastest-growing component of food production (>7%/year) (Lomartire and Gonçalves 2022; Duarte, Bruhn, and Krause-Jensen 2022; Moreira et al. 2022). Green seaweeds account for <0.1% of the total seaweed production (Bolton etal. 2016). Nevertheless, the ubiquitously distributed genus Ulva (Ulvales, Chlorophyta), widely known as sea lettuce, has received increasing attention. The distinct characteristics of the representative species of this ecologically and economically important genus are summarized in Figure 1, which indicates the immense potential of Ulva species in playing a central role in the rapidly emerging European seaweed aquaculture industry as they can be cultivated in both on- and off-shore conditions (e.g., Bolton et al. 2009; Mata et al. 2016; Steinhagen, Enge, et al. 2021). The most notable characteristics include world-wide coastal distribution, fast growth rates, relatively simple life cycle, ease of culture, historical use in food and feed, documented bioactivity and efficiency as a biological filter (Figure 1). Furthermore, it is the only species of macroalgae with a sequenced genome, which facilitates genetic transformation and presents the genus as an ideal model organism (Wichard etal. 2015; de Clerck etal. 2018; Blomme et al. 2023; Wichard 2023). 2.1. Ulva taxonomy and identification For most of taxonomic history, Ulva spp. have been discriminated using detailed morphological (blade shape or structure), anatomical (cell shape and size) and cellular (chloroplast position and appearance and the number of pyrenoids per cell) descriptions (Koeman and van den Hoek 1981). However, most species exhibit simple morphologies that are challenging to identify (Steinhagen et al. 2023; Hofmann etal. 2010; Kraft, Kraft, and Waller 2010), particularly due to phenotypic plasticity influenced by Figure 1. exceptional characteristics of the genus Ulva, demonstrating the reasons for its increased attention in diverse industries. High morphological plasticity: (Blomster, Maggs, and stanhope (1999); Hayden et al. (2003); wichard etal. 2015; steinhagen, weinberger, and Karez (2019); steinhagen etal. (2023); massive proliferation: (Charlier etal. (2006); Charlier, Morand, and Finkl (2008); smetacek and Zingone (2013); Gao et al. (2010); steinhagen weinberger, and Karez (2019)); high growth rates and ability to thrive at high stocking density: Mata, schuenhoff, and santos (2010); lawton et al. (2013); al-Hafedh, alam, and Buschmann (2014); sebök, Herppich, and Hanelt (2019); stedt, toth, et al. (2022); rapid nutrient uptake potential: Gao et al. (2013); shahar et al. (2020); rstedt et al. (2022); wide environmental tolerance: toth et al. (2020); Kirst (1990); Ghaderiardakani, Coates, and wichard (2017); Bao et al. (2022); thompson & Coates (2017); Ghaderiardakani et al. (2022); steinhagen, larsson, etal. (2022); simon, McHale, and sulpice (2022); steinhagen, enge etal. (2021); Kraft, Kraft, and waller (2010).
4 L. C. HOFMANN ETAL. environmental parameters (Wolf et al. 2012) and the microbiome (Wichard et al. 2015). To complicate matters, names initially used to describe European species are now used worldwide for species with different biogeographies, giving the impression that many Ulva species are cosmopolitan (Hughey etal. 2019 for the example of U. lactuca (Linnaeus, 1753)). In short, according to the ‘International Code of Nomenclature for Algae, Fungi, and Plants’ (Turland et al. 2018), the former Ulva fasciata is now correctly known as Ulva lactuca, and the former Ulva lactuca is now correctly known as Ulva fenestrata (Hughey et al. 2019). The correct identification of both parental wild stocks and cultivated Ulva spp. biomass is necessary, as the traits vary between the species (Fort et al. 2019; Olsson, Toth, et al. 2020; Olsson, Toth, et al. 2020; Cardoso et al. 2023), and is particularly important due to their prevalent application in commercial projects and industrial product labeling. In order to identify species and strains of particular commercial value, for example using species selection criteria, DNA barcoding, i.e., the amplification and sequencing of specific loci in the genome, must be used. With respect to EU legislation, the need for DNA barcoding to confirm the identity of commercially produced Ulva material is relevant, because only two species, Ulva lactuca, and the outdated genus “Enteromorpha” (Aonori), are is listed as acceptable non-novel food in the Novel Food catalogue of the Regulation (EU) 2017/2470 (Lähteenmäki-Uutela et al. 2021; Bolton, 2020; Barbier et al. 2019). Thus, several other Ulva species named differently may have been long used as foods and could also qualify for such status (Roleda etal. 2021; Barbier et al. 2019). Furthermore, several Ulva species are nuisance species in some coastal areas and negatively affect valuable coastal ecosystem functions when introduced to non-native areas (Charlier et al. 2006; Charlier, Morand, and Finkl 2008; Smetacek and Zingone 2013; Steinhagen, Weinberger, and Karez 2019; Fort, Mannion, etal. 2020). Therefore, correct species identification is critical to preventing invasive species propagation and introduction through aquaculture initiatives, and an integrative systematics approach is required to accurately identify Ulva spp., considering morphological characteristics, DNA sequencing of different markers, and species biogeography. However, due to a lack of algal barcode sequences from various geographical locations on public repositories (Bartolo et al. 2020) as well as sequence misidentifications in herbaria and online databases (Fort, McHale, et al. 2022), approximately 24–32% of foliose Ulva spp. in genetic databases are misidentified (Fort, McHale, etal. 2022). Thus, the taxonomy of Ulva, including identifying taxonomically valid names, species numbers and their circumscription, must be clarified using molecular methods with globally distributed specimens. Significant research has recently been conducted in Europe using foliose species, and currently both nomenclatural and taxonomic revisions of Ulva spp. are ongoing (Fort, McHale, et al. 2021; Fort et al. 2022; Hughey et al. 2019, 2020, 2021; Tran et al. 2022). Nevertheless, the names of Ulva species presented in this review should be taken with caution unless the authors have provided evidence of molecular identification confirmed by the type specimen. Possible alternatives to molecular approaches and their potential benefits and drawbacks, are comprehensively discussed by Tran et al. (2022). Future investigations would ideally facilitate molecular species identification without requiring sequencing, as proposed by Fort et al. (2021), who employed a restriction digest of the ITS1 PCR product to discriminate between the main foliose Ulva species. 2.2. Ulva production The FAO database reports data on the production of green seaweed, such as sea lettuce, since 1979. Various denominations can be found, such as bright green nori (Enteromorpha clathrata), green laver (Monostroma nitidum; Monostroma is a green macroalgal genus similar in form to Ulva, but not closely related), lacy sea lettuce (Ulva pertusa), and sea lettuces nei (Ulva spp.). The FAO database records aquaculture of sea lettuce for Ulva spp. in South Africa (3715 t in 2020), Monostroma nitidum in South Korea (8286 t in 2020), and Ulva prolifera (as Enteromorpha prolifera) in China (200 t in 2020). The annual production rates of these taxa are shown in Figure 2. The Republic of Korea’s 12,965 tonnes of green seaweed cultivation in 2019, including M. nitidum, Capsosiphon fulvescens, and Codium fragile, accounted for 78% of the global production. A recent report assessed that green macroalgae cultivation has recently decreased compared to the peak level of production, which occurred in the 1990s and early 2000s, depending on species (Cai 2021). This decrease can be seen in Figure 2, most notably for M. nitidum in South Korea and U. prolifera in China. The 16,696 tonnes of global green macroalgae production recorded in 2019 (approximately 0.05% of global macroalgae production) was less than half of the peak level in 1992 (38,556 tonnes), as opposed to the rapid growth in the production of brown macroalgae (3-fold) and red macroalgae (15-fold) between 1992 and 2019 (Cai 2021; FAO 2021). The reasoning behind this is unclear; however, recent statistics show that growth rates of total seaweed production in the leading Asian countries have slowed since 2015, potentially due to climate change, arrival at maximum carrying capacity, changes in marine spatial planning, and the aging seaweed farming workforce (Rieve, 2023). The 2,155 tonnes of Ulva produced globally in 2019 was also less than its peak production between 1950 and 2019, with 14,074 tonnes in 2008. The decline primarily reflects the decrease in Ulva prolifera (as Enteromorpha prolifera) production in China from 12,540 tonnes in 2008 to almost zero in 2019, whereas the global Ulva production in 2019 was 2,155 tonnes exclusively from South Africa (Table 1) (Cai, 2021; FAO, 2021). Nevertheless, the production numbers reported from South Africa may be overestimated, considering that only 2000 tons/year have been reported by Rothman etal. (2020). Because the Ulva is used as feed on farms rather than sold, production numbers are only estimates. Portugal has reported Ulvophyceae (the class of green algae that includes the genera Ulva and Monostroma) production in Europe since 2014; in 2019, this production reached 35 t (wet weight, FAO estimates). This IMTA-produced Portuguese alga has been identified as Ulva
CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 5 lacinulata (formerly U. rigida), a non-sporulating species that grows well in floating culture and contributes to green tide formation in some regions. Surprisingly, the FAO database does not list any Ulva production from Israel, despite its largest company (Seakura, Israel) producing 50 tons FW/ year. Within Europe, a recent assessment of the status of algal production in Europe reported 15 enterprises that cultivate Ulva spp. (Vazquez Calderon and Sanchez Lopez 2022). Nevertheless, not all European data are reported in the FAO database, which only includes data from Portugal and Spain. One of the leading European producers produced 150 tons of fresh weight in 2022, which is still only a fraction of the production rate (2000 tons/year) reported from abalone farms in South Africa (Bolton etal. 2016; Rothman et al. 2020). Considering that other countries may not be disclosing their production rates, the data currently available should be interpreted with caution and regarded as an underestimation. 2.3. Nutritional content The keywords “nutrient composition,” “Ulva,” “fatty acids,” “amino acids,” and “minerals” were searched through Scopus and Google Scholar to conduct a review on the nutritional content of Ulva spp. Special care was taken to include the species diversity of Ulva in all available data. The concentration ranges of proteins, carbohydrates, ash, lipids, amino acids, fatty acids, and minerals are summarized in Tables 2 and 3 and Supplementary Tables 1 and 2. In some cases, concentration ranges are provided, as well as seasonal variations when available. The biochemical profiles of different Ulva species are characterized by 13–50% ash, 5–27% protein, 0.5–4% lipids, and 53–78% total carbohydrates, of which 37–61% are fiber (data referring to dry weight (DW), Table 2). The protein content in sea lettuce is considered high among seaweeds; for instance, values >20% DW have been reported in Ulva reticulata and U. lactuca (Ortiz et al. 2006; Ratana-Arporn & Chirapart 2006) and can reach content >30%, more than double the natural content, when produced in nutrient-enriched environments (Viera et al. 2011). The levels found in high-protein terrestrial plants, such as soybeans, reach up to 40% DW (“USDA FoodData Central”). To measure the seaweed protein content, the nitrogen factor of 4.76 was used, which provides a lower nitrogen-to-protein ratio value (Angell et al. 2016). A conversion factor of 5 has been proposed to measure the nitrogen-to-protein ratio of seaweeds accurately. Figure 2. Global production of green seaweeds reported in the Fao database since the 1970s reported by country; grey, Ulva spp. in south africa; green, Ulva spp. in vietnam; blue, M. nitidum in south Korea; orange, U. prolifera in China; not visible due to insignificant amounts: Ulva spp. produced in Portugal and spain. Table 1. average and maximum global production of green seaweeds by country, 1950–2019 (Cai 2021; Fao 2022). Ulva species average annual production 1950–2019 (wet tonnes) Maximum annual production 1950–2019 (wet tonnes) Maximum annual production 1950–2019 (year) Cultivation in 2019 (wet tonnes) Cultivation in 2020 (wet tonnes) Cultivation in 2021 (wet tonnes) Country Monostroma nitidum 3,991 17,248 1992 6,321 8,241 7,958 republic of Korea Enteromorpha (Ulva) prolifera 1,367 12,540 2008 –*200 850 China Ulva spp. 515 2,900 2005 – 3,715 2,882 south africa Green seaweeds nei – – 2019 1,717 952 0 vietnam Green seaweeds nei 17.56 35 2019 35 5 5 Portugal Green seaweeds nei 0.35 0.87 2019 0.87 – – spain *Notes: “–” indicates zero or no data.
6 L. C. HOFMANN ETAL. The amino acid profiles of Ulva species are characterized by the predominance of aspartic acid, glutamic acid, and alanine (Supplementary Table 3) (Ferreira et al. 2021; Maehre et al. 2014; Peña-Rodríguez et al. 2011; Shuuluka, Bolton, and Anderson 2013). The values presented are standardized to % of protein where possible, but, strong variability between studies and differences in the units reported (% of protein vs. dry weight) make comparisons difficult, suggesting the need for a more systematic, standardized analysis (see future research directions). A principal component analysis (PCA) of the amino acid content of various Ulva spp. from various geographic regions and cultivation conditions showed that the first two components accounted for 78% of the variability. The first principal component was primarily influenced by glycine, serine, leucine, and tyrosine, while the second component was notably affected by cysteine. Cysteine was detected in only some species, resulting in significant separations between them in the PCA. Notably, U. capensis exhibited an exceptionally high concentration of glycine, U. fenestrata showed a high concentration of histidine, and U. clathrata displayed elevated levels of both arginine and glycine (Figure 3). The analysis also revealed co-occurrence patterns: glycine/serine (positive), leucine/tyrosine (positive), and cysteine/glycine (negative). In order to compare the nutritional quality of Ulva spp. to terrestrial plants, we conducted a PCA of the nutritional content of Ulva spp. presented in Table 2 and the nutritional content of soy, corn, rice and wheat from the USDA FoodData Central website. The results show that the Ulva spp. clustered more closely together than to the terrestrial plants, but all species clustered most closely to wheat, compared to corn, rice or soy (Figure 4). The protein and lipid content separated Ulva spp. most strongly from soy. The implications of these results are discussed in the section on future research directions below. The lipid content of Ulva is relatively low (0.5–4%). The predominant fatty acid is the saturated fatty acid (SFA) palmitic acid (16:0), making up an average of 27.8% in the species presented in this review. Ulva also contains monounsaturated and polyunsaturated (PUFA) fatty acids, particularly the essential linoleic acid (18:2 n-6) and linolenic acid (18:3 n-3) (Supplementary Table 2; Cardoso et al. 2017; Maehre et al. 2014; Neto et al. 2018; Lopes et al. 2019). The SFA/USFA ratio of all species presented is below 1 (0.15–0.90), with the exception of cultivated U. clathrata from a large-scale cultivated system, which had a ratio of 2.00. The MUFA/PUFA ratios ranged from 0.3 to 2.02 and the omega 6/omega 3 ratios ranged from 0.2 to 2.7. Wild collected U. fenestrata, U. lactuca and U. rotundata had the Table 2. nutritional composition of different species of Ulva. species season/Month Protein % Carbohydrate % lipid % ash% Moisture reference Ulva pertusa april nd nd 2.15 nd 83.32 (Floreto, teshima, and ishikawa 1996) U. reticulata May 21.1 55.8 0.75 17.6 22.5 (ratana-arporn and Chirapart 2006) U. clathrata nd nd 2.62 nd 92.00 (Kendel etal. 2015) U. lactuca 27.2 61.5 0.3 11.0 12.6 (ortiz et al. 2006) U. clathrata Mss 21.9 nd 2.5 49.6 nd (Peña-rodríguez et al. 2011)lss 20.1 nd 2.2 27.5 nd U. expansa 4.12 nd 0.65 35.66 84.59 (osuna-ruíz etal. 2023) U. prolifera 19.87 nd 6.06 17.50 nd (Pirian etal. 2016) U. flexuosa 10.55 nd 2.82 33.00 nd U. fasciata 14.06 nd 0.56 20.21 nd U. californica 15.20 nd 3.75 28.76 nd U. compressa 18.64 nd 0.90 22.30 nd U. lactuca 21.55 nd 0.75 12.18 nd U. linza 10.16 nd 3.70 24.62 nd U. rigida 16.6 56.4 3.7 25.2 82.09 (viera etal. 2011) U. rigida 33.8 40.5 4.4 21.5 82.0 (viera etal. 2011) U. rigida nd nd 0.8 nd nd (ivanova, stancheva, and Petrova 2013) U. fenestrata nd nd 0.5 nd nd (Colombo et al. 2006) U. fenestrata spring 20.79 32.21 3.2-3.55 16.6 82 (steinhagen, larsson, etal. 2022; steinhagen, enge etal. 2021) summer 4.67 40.21 1.17 22.56 81 U. fenestrata 17.8–23.2 nd nd nd nd (stedt, trigo, etal. 2022) U. fenestrata (as U. lactuca) 15%–21%*nd nd nd nd (roleda etal. 2021) U. linza nd nd 1.31 nd nd (Bakan et al. 2021) U. lactuca spring 20.12 44.81 4.09 22.08 8.9 (Khairy and el-shafay 2013)summer 17.88 46.42 3.57 17.56 14.57 autumn 16.78 42.09 3.14 23.19 14.8 U. lacinulataalab 11.08 32.66 7.00 17.08 83.57 Current authors U. compressablab 26.19 20.66 8.13 12.52 90.59 Current authors Ulva sp.cFall 23.87 9.36 3.12 20.06 83.75 Current authors *Calculated from total nitrogen using the conversion factor 4.6. Mss: medium scale system; lss: large scale system; nd: not determined. aFrom the north atlantic (Portugal). see Cardoso etal. (2023) for information on the origin of this strain and the molecular identification. bFrom the German wadden sea, dorum neufeld, (53.742433, 8.514724). cFrom the north east Harbor of Helgoland, Germany (54.184237, 7.890829).
CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 7 Table 3. Mineral composition of different species of Ulva. elements wet dried dried dried winter spring summer autumn winter spring summer autumn June spring summer Macro elements (mg/g) U. rigida U. clathrata U. fenestrata U. fenestrata Ca 0.69 3.23 0.46 1.11 2.11 12.73 1.56 2.23 nd 9.05 18.80 nd nd 1.5–1.8 K 5.66 6.09 4.68 7.18 7.01 7.19 6.52 8.17 nd nd nd nd nd 16–18 Mg 5.97 8.41 5.69 8.92 10.55 8.91 6.13 10.22 nd nd nd nd nd 15–17 na 5.19 5.74 4.44 4.62 6.27 6.31 5.83 5.21 nd nd nd nd nd 17–22 Micro elements (µg/g) al 89.00 60.00 44.93 110.80 158.00 211.87 171.73 224.60 nd nd nd 27.446 36.727 nd B 17.67 15.53 52.27 33.53 36.87 34.73 59.40 45.93 nd nd nd nd nd nd Ba 0.53 0.80 0.67 0.80 0.60 1.27 0.87 1.67 nd nd nd nd nd nd Co <0.035 <0.035 <0.035 <0.035 <0.035 <0.035 <0.035 <0.035 nd nd nd <0.035 0.039 nd Cr <0.010 0.20 0.60 0.20 <0.010 0.20 0.07 <0.010 nd 0.52 0.80 0.047 0.15 nd Cu 3.27 3.00 2.00 1.33 6.33 4.13 1.00 1.93 1.6 54.17 13.80 0.482 0.74 11–26 Fe 227.87 188.20 124.60 225.07 293.93 461.47 574.53 399.87 130 340.1 41.72 25.89 35.56 30–60 Mn 3.00 3.07 4.60 5.40 5.47 10.07 10.27 6.93 8.4 nd nd 1.29 4.77 5–14 ni <0.035 <0.035 <0.035 <0.035 <0.035 <0.035 <0.035 <0.035 nd 2.37 5.72 0.084 0.348 nd Zn 13.20 8.47 2.00 4.40 20.13 17.60 13.80 14.40 1.0 188.91 16.66 1.59 1.52 5–14 reference (Beril and Çankırılıgil 2019)(Queirós etal. 2021)(Peña-rodríguez etal. 2011)(steinhagen, larsson, etal. 2022)(roleda et al. 2021) nd: not determined. highest omega-3 fatty acid content and U. fenestrata and U. rotundata had the highest UFSA/FSFA ratios. A PCA of the fatty acid data, which grouped species by morphology (tubular, foliose, or both), indicated that many blade-forming species clustered together (Figure 5). On average, these foliose species (blades) exhibited higher total PUFA and SFA levels than the tubular species. Ulva clathrata was distinctive due to its particularly low MUFA content. Ulva lactuca demonstrated high variability, likely stemming from misidentification. Given that U. lactuca is not found in Europe, the data presented by van Ginneken etal. (2011) probably pertain to Figure 3. a principal component analysis of the amino acid profiles (% of protein) of various Ulva spp. from different geographic regions and cultivation conditions. data are taken from supplementary table 3 and analyzed using JMP® pro v. 17 (sas institute inc., Cary, nC, usa). Prior to analysis, data underwent a log + 0.1 transformation. the “contrib scale” indicates the contributions (in percentage) of the variables to the principal axes. lss: large scale system; Mss: medium scale system (Peña-rodríguez etal. 2011). arg: arginine; ala: alanine; asp: aspartic acid; cys: cysteine; gly: glycine; glu: glutamic acid; his: histidine; ile: isoleucine; leu: leucine; lys: lysine; met: methionine; phe: phenylalanine; pro: proline; thr: threonine; tyr: tyrosine; ser: serine; val: valine. Figure 4. Principle component analysis (Martin and Maes 1979; Becker and venkataraman 1984; venables 1997) of the nutritional content (ash, protein, lipids, carbohydrates) of different Ulva spp. and soy, corn, rice and wheat. data for Ulva were taken from table 2 as percentages. when single values were missing, mean values were used. data for soy, corn, rice and wheat were taken from the united states department of agriculture food data Central website (https://fdc.nal.usda.gov/index.html.) as percentages. the analysis was performed using the environment of r (version 4.02.), rstudio (version 2022.02.3). data were not transformed prior to analysis. Percentages were transformed by arcsine-square-root transformation to correct for deficiencies of the proportions in normal distribution.
14 L. C. HOFMANN ETAL. Table 4. summary of the effect of Ulva-supplemented aquafeed on different cultivated seafood. examined organism species inclusion rate (% of dw) time (weeks) weight gain and growth rate FCr Per PPv Protein utilization other impacts ref. african catfish (Clarias gariepinus) U. lactuca 10, 20, 30 10 decreased under diets of >10% impaired under diets of ≥20% decreased under diets of ≥20% decreased decreased diet palatability at high inclusion rate (≥20%) 1 Common Carp (Cyprinus carpio)U. rigida 5, 10, 15, 20 16 decreased only under diet of 20% impaired only under diet of 20% n.s. 2 nile tilapia (Oreochromis niloticus) U. lactuca 5, 10 9 n.s. n.s. n.s. 3 nile tilapia (Oreochromis niloticus) U. intestinalis 10, 20, 30, 40, 50 6n.s. under diet ≤30% but decreased at higher inclusion rates n.s. n.s. 4 nile tilapia (Oreochromis niloticus) Ulva spp. (iMtacultured) 10, 15, 20 9n.s. under diet of 10% but decreased at higher inclusion rates n.s. under diet of 10% but impaired ≥15% decreased under diets of ≥15% Highest lipid content in fish flesh under diet with 20%; no apparent effect on diet palatability 5 nile tilapia (Oreochromis niloticus) Ulva sp. 5, 10, 15, 20, 25 increased under diets of ≤15%, decreased under diet of 25% improved under diets of ≤15%; no change under other diets increased under diets of ≤20% increased under diets of 10–25% 6 nile tilapia (Oreochromis niloticus) U. spp. 10 12 n.s. n.s. n.s. 7 nile tilapia (Oreochromis niloticus) U. rigida and U. lactuca 1:1 10, 15, 20 9decreased under diets of >10% impaired under diets of ≥15% increased under diets of ≥15% 8 nile tilapia (Oreochromis niloticus) U. rigida 10, 20, 30 11 decreased only under diet of 30% n.s. but increased under diet of 30% decreased only under diet of 30% 9 nile tilapia (Oreochromis niloticus) U. rigida 5 16 improved improved increased increased 10 nile tilapia (Oreochromis niloticus) U. rigida 5, 10, 15 12 decreased only under diet of 15% impaired only under diet of 15% increased only under diet of 15% 11 striped mullet (Mugil cephalus)U. lactuca 10, 15, 20, 25 15 improved with increasing inclusion rate improved with increasing inclusion rate increased with increasing inclusion rate 12 Gilthead seabream (Sparus aurata) U. lactuca 5 8 n.s. n.s. n.s. 13 Gilthead seabream (Sparus aurata) U. lactuca (iMta-Ulva) 2.6, 7.8, 14.6, 29.1 16-20 decreased only under diet of 29.1% n.s. but impaired under diet of 29.1% decreased 14 Gilthead seabream (Sparus aurata) U. rigida 5, 15, 25 10 n.s. but improved under diet of 30% n.s. 15 (Continued)
CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 15 examined organism species inclusion rate (% of dw) time (weeks) weight gain and growth rate FCr Per PPv Protein utilization other impacts ref. Gilthead seabream (Sparus aurata) U. rigida 5 (+incresing lipid content) 7n.s. but improved under a high-lipid diet (22%) n.s. but improved under a high-lipid diet (22%) n.s. n.s. 16 red seabream (Pagrus major)U. pertusa 5 6 n.s. n.s. n.s. 17 Black seabream (Acanthopagrus shlegeli) U. pertusa 10 20.5 n.s. 18 rainbow trout (Oncorhynchus mykiss) U. rigida 10 12 decrease (only after starvation) 19 rainbow trout (Oncorhynchus mykiss) U. lactuca or U. linza 10 8.5 decreased 20 european seabass (Dicentrarchus labrax) U. lactuca 5, 10, 15 8decreased when content in feed incresed impaired when content in feed incresed increased 21 european seabass (Dicentrarchus labrax) U. rigida 5 10 decreased when content in feed incresed impaired when content in feed incresed n.s. 22 european seabass (Dicentrarchus labrax) U. lactuca 5, 10, 15 8improved under diets of ≤10%; decreased at 15% improved under diets of ≤10%; impaired at 15% increased only under diet of 5% increased only under diet of 5% 23 european seabass (Dicentrarchus labrax) 10 4 decreased n.s. inhibitory of protein digestion 24 white-spotted snapper (Lutjanus stellatus) U. lactuca 5, 10, 15, 20 8.5 n.s. n.s. reduced pepsin and lipase activity in the gut under diets of >5% 25 senegalese sole (Solea senegalensis) U. ohnoi 5 13 decreased n.s. 26 senegalese sole (Solea senegalensis) U. ohnoi 6 13 n.s. n.s. selective retention of n-3 PuFa, ePa & dHa; positive effect on fish fillet texture & color. Positive effects maintained over a long period after supplementation 27 senegalese sole (Solea senegalensis) U. ohnoi 5 decreased 28 large yellow corvina (Larimichthys polyactis) U. prolifera 5, 10, 15 10 improved when content in feed incresed n.s. decreased when content in feed incresed 29 Goldfish (Carassius auratus)U. reticulata 2, 4, 6, 8 6 improved improved haematological parameters and fish color 30 sea chub (Girella laevifrons; Kyphosidae) U. lactuca 15, 30, 45 4n.s. under diet of 30%; decreased under other diets 31 dusky kob (Argyrosomus japonicus; sciaenidae) Ulva. sp. 5, 10, 15, 20 9 decreased impaired 32 Pacific white shrimp (Litopenaeus vannamei) U. lactuca 1, 2, 3 4 improved improved Higher content of lipid and carotenoid in shrimp flesh under 3% diet 33 Table 4. Continued. (Continued)
16 L. C. HOFMANN ETAL. examined organism species inclusion rate (% of dw) time (weeks) weight gain and growth rate FCr Per PPv Protein utilization other impacts ref. Pacific white shrimp (Litopenaeus vannamei) U. lactuca (iMta-Ulva) 25, 50 (fresh Ulva for replacing aquafeed) 7n.s. under diet of 25%, decreased under the diet of 50% improved (due to the reduced aquafeed in the diets) low protein content in shrimps flesh (although Ulva contained 32% protein as in the aquafeed) 34 Pacific white shrimp (Litopenaeus vannamei) U. lactuca 6.35, 12.7, 19.05, 25.4 6decreased under diets of >6.35% impaired under diets of ≥19.05% decreased under diets of >6.35% low energy, protein, and amino acid digestibility (compared with fishmeal or soybean meal) 35 abalone (Haliotis midae)Ulva sp. (iMta-Ulva) 20, 30, 40, 60 (replaced commercial aquafeed) 52 n.s. unique associations in the gut microbiome and a lower abundance of Vibrio sp. 36 abalone (Haliotis asinina)U. pertusa 2.7, 5.4, 8.1 17.5 n.s. n.s. n.s. 37 abalone (Haliotis discus)U. australis 4, 8, 12, 16, 20 (replaced Unidaria pinnatifida) 2.5 improved reduced mortality after exposure to air 38 abalone (Haliotis laevigata)Ulva sp. fresh or enriched Ulva as sole feed compared to commercial aquafeed 13 decreased impaired decreased enriched Ulva improved growth compared with non-enriched Ulva 39 abalone (Haliotis laevigata)Ulva sp. 5, 10, 20 13 improved 39 abalone (Haliotis tuberculata)Ulva rigida enriched Ulva, non enriched macroalgae 12 improved improved decreased enriched Ulva improved growth compared with non-enriched Ulva 40 abalone (Haliotis tuberculata)U. rigida Young and old U. rigida’s effect on abalone post larval growth 4 improved old and young U. rigida germlings with U. lens germlings improved postlarval growth 41 Purple sea urchin (Arbacia punctulata) U. lactuca Fresh Ulva and commercial fish diets 12 n.s. increased gonads mass and altered their color; reduced alimentary canal index (% of total mass) 42 Collector sea urchin (Tripneustes gratilla elatensis) U. fasciata (iMta-Ulva) Fresh Ulva as sole feed and Gracilaria sp. or algal-free pellets 8 improved Positive effect on the gut microbial networks and occurrence of unique microbes related to metabolism of Ulva polysaccharides 43 Collector sea urchin (Tripneustes gratilla) U. rigida (iMta-Ulva) 5, 15, 20 in the pelleted diet 12 n.s. improved diet palatability, consumption, and digestibility (compared with algal-free pellets); increased gonads somatic index (compared with fresh Ulva diet) 44 Collector sea urchin (Tripneustes gratilla) U. pertusa Fresh Ulva as sole feed and Undaria or Gloiopeltis decreases compared with Undaria but better than Gloiopeltis improved 45 Collector sea urchin (Tripneustes gratilla lineus) U. armoricana Fresh Ulva, or in pelleted diet (20%) improved Ulva diets eliminated the need for a high-protein diet. Ulva-containing pellets during the 12 weeks prior harvesting is necessary for improving gonad size and color 46 Table 4. Continued. (Continued)
CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 17 performance (Morais et al. (2020); the information is scarce). The main drawbacks to using U. lactuca in ruminant diets are frequently cited as their low dry matter and high ash content (Tayyab et al. 2016) and low effective degradability (41% for organic matter degradability) values (Arieli, Kissil, and Sklan 1993). The high mineral content of seaweeds restricts their net, digestible, and metabolizable energy values and gross energy content. Ulva has been regarded to be nearly equivalent to a low-to-moderate quality forage and ideal to be used with feeds that have a high energy/low protein content like cereal crops (Arieli, Kissil, and Sklan 1993). Samara et al. (2013) reported that 3%–5% (DM) of Ulva lactuca could be safely supplemented to lambs without negatively affecting blood water balance, liver, or kidney functions. However, feeding rams a lamb diet supplemented with intact Ulva lactuca did not positively affect growth performance, thermoregulatory responses, or plasma oxidative status, whereas feeding lambs intact Ulva lactuca negatively affected rams’ seminal and testicular characteristics, which were more pronounced at 5% than at 3%. Male lambs can consume up to 20% U. lactuca in a diet composed primarily of vetch hay or concentrate without negatively affecting the diet’s flavor. It had a moderate energy digestibility (60%) and a low (40%) protein degradability (Arieli, Kissil, and Sklan 1993). El-Waziry et al. (2015) reported that U. lactuca supplementation did not affect sheep growth, in vitro gas production, potential degradability, estimated energy, organic matter digestibility, or microbial protein synthesis. Furthermore, Ventura and Castañón’s (1998) concluded that U. lactuca is a high-protein, medium-quality forage for goats. In a different study (Rey-Crespo, López-Alonso, and Miranda 2014), adding a seaweed blend (Ulva rigida, Laminaria ochroleuca, Saccharina latissima, Saccorhiza polyschides, Mastocarpus stellatus, and Sargassum muticum) to the diets of dairy cows at a rate of 100 g/cow/day increased the amount of iodine in the milk. This suggests that incorporating seaweed into the diet is a viable method of increasing iodine levels in milk. Although various results have been reported with variable effects on rumen fermentation, Ulva has shown promising potential for reducing ruminal methane production in vitro (Dubois etal. 2013; Machado etal. 2014; Kinley etal. 2016). When incubated at 25%, Ulva sp. significantly decreased methanogenesis from 101 mL g−1 DM to 86.2 mL g−1 DM compared to the control; however, the effect on methane production depended on the substrate because all seaweeds decreased methane production when combined with hay, but only Gigartina sp. reduced methane production when incubated with corn silage (Maia et al. 2016). Recently, Ulva sp. was the only macroalgae species tested that did not reduce methane production (Mihaila et al. 2022), suggesting that more research is needed to reach a more conclusive result regarding the impact of Ulva spp. on methane production. 5.2. Monogastric terrestrial animals (swine, cuniculus) Recently, seaweeds have been included in low amounts (1–2% for the potential benefits to pig health and meat examined organism species inclusion rate (% of dw) time (weeks) weight gain and growth rate FCr Per PPv Protein utilization other impacts ref. Purple sea urchin (Paracentrotus lividus) Ulva sp. 50 (fresh Ulva for replacing pelleted feed) 46 Purple sea urchin (Paracentrotus lividus) U. lactuca (iMta-Ulva) Fresh Ulva and Gracillaria compared to pelleted diet 13 n.s. improved gonads color but reduced gonad somatic index 47 sea cucumber (Holothuria scabra) U. lactuca raw vs. mechanically shredded Ulva 0.5 n.s. Higher feed ingestion and fecal production rates under the shredded Ulva diet 48 sea cucumber (Apostichopus japonicus) U. lactuca 5, 10, 40 in pelleted diet 12 improved with increasing feed content improved with increasing feed content Higher attractiveness and intake of 40% Ulva diet. lower performances compared with soybean-containing diet 49 sea cucumber (Apostichopus japonicus) U. lactuca 14, Laminaria at same rate or algal free pellets decreased compared with Laminaria lower content of n-3 PuFa in flesh than in Laminaria diet 50 n.s.: no significant change; dw: dry weight; FCr: food conversion ratio; Per: protein efficient ratio; PPv: protein productive value. 1(abdel-warith, Younis, and al-asgah 2016); 2(diler et al. 2007); 3(natify etal. 2015); 4(siddik and anh 2015); 5(Marinho etal. 2013); 6(el-tawil, 2010); 7(silva etal. 2015); 8(Marinho etal. 2013); 9(azaza et al. 2008); 10(ergün etal. 2009); 11(Kut Güroy et al. 2007); 12(wassef, el Masry, and Mikhail 2001); 13(Guerreiro etal. 2019); 14(shpigel et al. 2018); 15 (vizcaíno etal. 2016); 16(emre etal. 2013); 17(Mustafa, 1995); 18(nakagawa, Kasahara, and sugiyama 1987); 19(Güroy etal. 2011); 20(Yildirim etal. 2009); 21(wassef, el-sayed, and sakr 2013); 22(valente etal. 2006); 23(wassef, 2005); 24(Martínez-antequera etal. 2021); 25(dashi Zhu etal. 2016); 26(Cerezo etal. 2022); 27(sáez etal. 2020); 28(vizcaíno etal. 2019); 29(asino, ai, and Mai 2011); 30(rama nisha etal. 2014); 31(Cruz, 2019); 32(Madibana etal. 2017); 33(elizondo-González etal. 2018); 34(laramore etal. 2018); 35(Qiu, neori, etal. 2017); 36(Macey, 2021); 37(santizo-taan, Bautista-teruel, and Maquirang 2020); 38(ansary et al. 2019); 39(Bansemer, Qin, Harris, duong, Hoang, etal. 2016)40 (Bansemer, Qin, Harris, duong, Currie, etal. 2016); 41(de viçose etal. 2012); 42(suckling etal. 2022); 43(Masasa etal. 2021); 44(Cyrus etal. 2015); 45(Floreto, teshima, and ishikawa 1996); 46(Cyrus etal. 2015); 47(Prato etal. 2018); 48(shpigel et al. 2018); 49(irfan etal. 2022); 50(Joaquina ibarra-arana et al. 2018); 51(anisuzzaman etal. 2018). Table 4. Continued.
18 L. C. HOFMANN ETAL. quality (Mišurcová, 2011). A new feed supplement containing Ulva enriched with Zn (II) and Cu (II) as a dietary source of microminerals for pigs showed higher bioavailability than an inorganic salt control when fed to piegs (Michalak, Chojnacka, and Korniewicz 2015). Furthermore, an algae–clay-based complex made from Ulva sp., Solieria chordalis, and montmorillonite clay increased the ileal digestibility of energy and essential amino acids when added to the diets of growing pigs (Suarez and Gallissot 2016). A study using an in vitro system of porcine intestinal epithelial cells showed that ulvan from Ulva armoricana upregulated the gene expression of cytokines such as IL1, IL6, IL8, and TNF (Berri et al. 2017, Bikker et al. 2016). The immunomodulatory effect of Ulva armoricana was evaluated in sows by Bussy et al. (2019). The higher dietary level increased anti-Bordetella IgG in the sow’s blood and colostrum, whereas with the middle dietary integration, IgA increased in milk. Thus, based on digestibility, Ulva may be a better feed ingredient for pigs than for poultry (see below), whereas the extracted fraction seems a promising ingredient for further evaluation in both organisms. Based on the essential amino acid content and in vitro nitrogen (85%) and organic matter (90%) digestibility, the extracted fraction seems a promising protein source in diets for monogastric animals with improved characteristics compared to intact Ulva (Bikker et al. 2016). Furthermore, a recent study has found that enzymatic supplementation with carbohydrase, such as the recombinant ulvan lyase, may exacerbate the indigestibility effects observed from feeding U. lactuca alone to piglets (Ribeiro et al. 2024). Studies investigating the effect of Ulva-supplemented diets on other terrestrial animals are rare; however, meal supplemented with low amounts (1%) of Ulva have shown positive effects on the growth performance and diet digestibility in rabbits, with no negative hematological or biochemical effects on rabbit health (El-Banna et al. 2005). 5.3. Poultry Several studies have investigated the influence of Ulva spp. as a feed additive on chicken development and/or carcass characteristics (Matshogo, Mnisi, and Mlambo 2020; Abudabos et al. 2013; Nhlane et al. 2021; Thavasi Alagan et al. 2020; Ventura, Castañon, and McNab 1994). Most studies have shown that Ulva spp. can be used at low inclusion levels (<10%) without any suppression in the growth performance of chickens. Green seaweed meal derived from U. lactuca at 0, 2, 2.5, 3, and 3.5% had no adverse effect on the growth performance, visceral organ size, carcass characteristics, and meat quality of indigenous Boschveld chicken (Nhlane et al. 2021). Similarly, the addition of Ulva-based green seaweed meal (0, 20, 25, 30, and 35 g kg−1) had no significant effect on the growth performance of broiler chickens; however, increases in various meat shelf-life indices were observed (Matshogo, Mnisi, and Mlambo 2020). Furthermore, corn can be replaced with 3% U. lactuca without affecting growth performance while improving the dressing percentage and breast muscle yield (Abudabos et al. 2013). In addition, broiler diets can be supplemented with U. lactuca without affecting health and growth performance (Nhlane etal. 2021). Ventura, Castañon, and McNab (1994) concluded that feeding U. rigida beyond 10% in the diet reduces the feed intake and suppresses the growth performance of broiler chickens, suggesting that Ulva supplementation levels should remain below 10%. Using Ulva spp. in chicken feed at high concentrations is likely restricted because fiber fractions of indigestible algal cellulose and hemicelluloses (Øverland, Mydland, and Skrede 2019), which primarily consist of gel-forming ulvan and insoluble cellulose, as well as trace amounts of glucuronans and xyloglucan (Lahaye and Robic 2007), may impair nutrient digestibility, suppressing growth performance (Kraan, 2012). Enriched ash content can also make seaweeds inappropriate for animal diets, especially monogastric animals, at higher concentrations. In contrast, microalgae have been suggested to be a promising alternative feedstock for livestock and poultry (Saadaoui et al. 2021). Nevertheless, the scale and cost of production needed and potential competition with human consumption present limitations for microalgae in feed as well. The major benefit of using macroalgae for feed is that biomass from algal blooms which is unsuitable for human consumption could be valorized for feed. Therefore, advanced procedures, which can decrease ash content and improve digestibility are needed to improve the acceptable feed components from Ulva spp. Digestibility can be improved by enzymatic hydrolysis with appropriate agents for seaweed species since the chemical makeup of seaweeds is different from that of terrestrial plants. Carbohydrate-active enzymes (CAZymes) have emerged as a promising alternative to destroy the Ulva spp. cell wall due to the efficacy of these enzymes in hydrolyzing Ulva spp. material for protein and carbohydrate extractions (Batista etal. 2020; Postma etal. 2018). Moreover, CAZymes have demonstrated carbohydrate action in microalgae cell walls (Coelho etal. 2020). Thus, the degradation of seaweed biomass with feed enzymes would optimize their utilization as feedstuffs to partially replace unsustainable and conventional sources, such as maize and soybean meal (Costa etal. 2021). Costa etal. (2022) conducted a trial on broiler chickens to study the influence of U. lactuca (15%) with and without enzyme addition (carbohydrase), indicating that 15% U. lactuca resulted in no harmful effects on growth performance and improved meat quality because of antioxidant influence, mineral, and PUFA (n-3) accumulation. Another study assessed the pretreatment of edible seaweed (Ulva spp.) with a mixture of proteolytic and fibrolytic enzymes on the physical and meat quality characteristics of broiler chickens (Matshogo, Mnisi, and Mlambo 2021), demonstrating that seaweed pretreatment with the enzyme mixture did not affect feed consumption, physiological responses, and carcass characteristics of broiler chickens. In contrast, a co-product of Ulva laetevirens (synonomous with U. australis) exposed to a wide endo-protease supplementation in a broiler’s diet showed no distinct effect on their growth performance, whereas protease pretreatment masked or suppressed the health-promoting bioactive substance of U. laetevirens (Stokvis et al. 2022). Ulva laetevirens
CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 19 improved the feed conversion rate of broiler chickens and reduced the digestibility and villus height, whereas protease pretreatment failed to improve growth performance and other health-related traits. It is critical to obtain a better knowledge of how the nutritional components of Ulva spp. behave in in vitro digestibility tests and the digestive tract of broiler chickens to explore the impacts of Ulva inclusion in poultry diets. Given the protein content of wild Ulva, it can be concluded that wild Ulva is not a good source of protein (compared to any major vegetable protein source used in animal diets) and the presence of structural carbohydrates (usually referred to as fiber) limits the use of Ulva in diets for monogastric animals (poultry and pigs). Nevertheless, Ulva can be used in ruminant (cow, sheep, and goat) diets, however, studies are still underway since the fate of sulfonated carbohydrates is not yet known. 6. Beyond food and feed – Ulva in biomaterials In 2019, the seaweed hydrocolloid industry was valued at 1.74 billion USD. Nearly 50 years of seaweed bioprospecting have resulted in over 3,000 marine natural products or bioactive molecules from seaweeds (Ferdouse etal. 2018). While green seaweeds do not contribute to the hydrocolloid industry and only approximately 8% of the marine natural products or bioactive molecules come from green seaweeds (Ferdouse et al. 2018), they still demonstrate significant potential in biomaterials industries, particularly due to the presence of ulvan. Ulvan has attracted increasing attention in the last decade, considering that less than five papers on ulvan were published annually during 2000–2009, but more than 35 papers were published in 2019 (Cindana Mo’o etal. 2020). The benefits and potential of ulvan in diverse biotechnical applications have already been thoroughly reviewed by several authors (Kidgell et al. (2019) for review); therefore, ulvan was not the focus of this section. However, we provide insights into the potential use of Ulva in other biomaterials, including packaging, which is comprehensively discussed below. 6.1. Packaging (packaging films and packaging materials) The new circular economy plan, which is pivotal in the European Green Deal, EC’s agenda, and UNSDGs for sustainable growth, includes designing sustainable products, empowering consumers, and improving reuse in production processes. Some key product value chains include packaging, plastics, textiles, construction, food, water, and nutrients. Thus, to meet these initiatives and those for protecting and restoring the marine environment, new production concepts are required to address the growing demand and provide sufficient quantities of high-quality materials and food in the future (Eroldoğan et al. 2022). Over half of the plastics made are only used once (Gross, 2017), and over 99% of plastic packaging is produced from petroleum-based sources (Arrieta et al. 2017). Rethinking and redesigning sustainable packaging materials using natural resources to replace single-use plastics will be essential to achieving the new circular economy action plan (European Commission 2022). Marine resources, including seaweed, provide an enormous pool of yet unexplored and potentially valuable resources for producing diverse biomaterials, including packaging, and interest is growing in the use of macroalgae in the packaging industry. The global seaweed-based packaging market is expected to account for $613.42 million USD by 2029 (Data Bridge Market Research). Diverse types of films for food packaging have recently been developed (Abdul Khalil et al. 2017; Amin 2021; Gomaa etal. 2022; Ganesan, Shanmugam, Palaniappan, et al. 2018) from macroalgae-derived sources. Considering Ulva, most packaging biofilms are produced by extracting ulvan and combining it with a plasticizer, such as polyethylene glycol (PEG), sorbitol, or glycerol (Davoodi, Milani, and Farahmandfar 2021; Guidara et al. 2019, 2020). In some cases, ulvan is combined with another natural material, such as cellulose extracted from the same species (Gomaa et al. 2022) or red algal polysaccharides (Ganesan, Shanmugam, and Bhat 2018; Ganesan et al. 2018). In many cases, ulvan addition to the packaging film increased the film’s antioxidant activity (Amin 2021; Gomaa et al. 2022; Ganesan et al. 2018), suggesting that such seaweed-based packaging films may increase the shelf-life of certain packaged products. Currently, most packaging products are produced from brown or red algae (e.g., products from Evoware (biodegradable, edible seaweed-based packaging), AMAM (agar plasticity), Ooho (edible water packets from seaweed extracts), Loliware (seaweed-based cups and straws), Algopack (brown-algae based bioplastics), Kelpn (kelp-based bioplastic), and Janoodam (seaweed-based bowls and lids)). To our knowledge, the only known Ulva-based packaging products are produced by the company Eranova (https:// eranovabioplastics.com/technology/?lang=en), by enriching the content of starch, which is then extracted using an enzymatic cracking technique and then processed into biodegradable or durable bioplastic. However, some of the authors of the current work are presently conducting research to develop a sustainably produced, biodegradable, edible seaweed-based packaging material for the fast-food industry using mixtures of macroalgae biomass. This process requires no extraction, and is essentially waste-free. An initial screening of local seaweed species for packaging functionality led to testing and cultivating several species for seaweed-based packaging. Depending on the type and mixture of seaweed used and the applied preparation technologies (e.g., grinding), different material properties of the produced macroalgal-based packaging can be achieved. For example, the particle size distribution and film-forming abilities of the packaging material vary and have different material characteristics, such as lower or higher porosity, thicker and stronger films, or different material strengths. In external beta testing of the prototype with food products (baked fish and potato salad), 79–91% of customers rated the edible macroalgae packaging as good to very good (Bosse and Hofmann 2020). Based on these results, different types of packaging material can be developed for different functional uses,
20 L. C. HOFMANN ETAL. including in industries outside of food, by altering the seaweed species and their respective combinations. To our knowledge, this is the only seaweed-based packaging that uses 100% of the seaweed biomass and requires no extraction method. Further trials are currently underway to test different methods of packaging production from seaweeds (e.g., fiber casting or natural fiber injection molding). Nevertheless, one of the biggest hurdles, as in other industries, remains to be the processing and transport step from raw biomass to packaging production. The properties of Ulva that are conducive to packaging production (e.g., high cellulose and starch content) also make the seaweed a potential candidate for paper production. A recent study has shown that Ulva biomass can be successfully incorporated into filter paper at a concentration up to 4% without weakening the strength of the fiber network, and successfully removed pollutants (Cr, Cu, total Fe and Zn) due to its adsorbant properties (Caprita, Ene, and Cantaragiu Ceoromila 2021). 6.2. Plant biostimulants Biostimulants promote plant processes, including nutrient uptake efficiency, stress tolerance, and crop quality (Regulation (EU) 2019/1009 of the European Parliament), and reduce the demand for inorganic inputs (Shukla et al. 2019). Currently, macroalgae are involved in 37% of the biostimulant market (Rouphael and Colla 2018) and contain classes of compounds, such as betaines, phenols, and polysaccharides, which are biostimulants (Stengel, Connan, and Popper 2011). The main temperate macroalgae-sourced biostimulant products (e.g., Maxicrop) are almost exclusively produced from the brown wild-harvested species Ascophyllum nodosum (www.solabiol. com/en/principles-maxicrop). In addition, Ecklonia maxima is used to produce the biostimulant Kelpak (https://www.kelpak. com/eckloniamaxima.html), which is exported globally. The red, tropical macroalgae Kappaphycus alvarezii has also been extensively studied (Kumar etal. 2020; Sahana etal. 2022; van Tol de Castro etal. 2023; de Araújo Amatuzzi etal. 2020) and is also commercially available as a biostimulant (e.g., www. prospersea.com). Ulva spp. also have biostimulant properties, although there are little studies to date for green macroalgae compared to brown and red macroalgae. Ulva extracts improve salinity stress response (El Boukhari et al. 2021; Hussein etal. 2021; Latique etal. 2021), drought tolerance (Li et al. 2020), growth (Castellanos-Barriga etal. 2017; Hassan etal. 2021; Hussein et al. 2021; Mendoza-Morales et al. 2019; Michalak et al. 2016; Osuna-Ruíz et al. 2023), antioxidant activity (Osuna-Ruíz et al. 2023; Ennoury et al. 2022; Latique et al. 2021), and plant flavors (Paulert et al. 2021). Using Ulva spp. extracts as a biostimulant source increases crop yield and contributes to global food security while also creating another product route for some biomass produced during green tides (Shefer etal. 2022). While first plant trials using biochar produced from Ulva spp. have shown variable effects on plant growth (Kenneth et al. 2022; Roberts and de Nys 2016), this research field is still in its infancy, and finding solutions to reduce the sodium content in seaweed-based biochar will be a challenge for the future. 6.3. Biorefinery Biorefineries use a biomass processing approach that facilitates the production of several value-added products from a given biomass feedstock (crops, lignocellulosic biomass, seaweed, microalgae, and insects) and ensure the full usage of resources, leading to zero waste and minimal greenhouse gas emissions (Barragán-Ocaña et al. 2023). By producing multiple products from the same raw materials, biorefineries increase the revenue per mass of feedstock, and diversify applications, making the whole system economically resilient (Golberg et al. 2020). The co-production of multiple products usually requires multiple subsequent processing steps produces one or several different products (Golberg et al. 2020). In an Ulva biorefinery, the separation of salt, cellulose, ulvan, starch, proteins, lipids, simple monosaccharides, and peptides has been reported in various process configurations (Table 5). High protein yields from Ulva can be obtained after extracting salt and ulvan from the seaweed (Magnusson et al. 2019), and extracting protein and water-soluble molecules in the first step increases the content and purity of residual water-soluble polysaccharides such as ulvan (Golberg et al. 2020). This is critical because achieving a certain level of concentration and purity is a major economic and technological hurdle for biorefineries. In addition, certain processes, such as crushing, milling, and other cell and tissue disruptions, usually benefit most subsequent processes by improving the biomass contact surface and the accessibility of intracellular components without intermediate drying. Therefore, the energy and cost of such processes benefit the entire processing chain rather than a single product (Zollmann et al. 2019). Although thermochemical approaches using high temperatures and solvents continue to be used at industrial scales to obtain different seaweed-derived products, more environment-friendly techniques to better preserve the product’s quality and functionality are emerging, including enzyme-, microwave-, or ultrasound-assisted extraction, supercritical fluid extraction, pressurized solvent extraction, pulsed electric fields, or ohmic heating (Matos et al. 2021). 6.4. Knowledge gaps and future challenges Currently, biorefinery design is a major challenge, i.e., choosing the processes and equipment and integrating them into one optimized process flow (Golberg et al. 2020) because biomass processes and equipment are usually designed to solely produce one product and not preserve the byproducts for subsequent processing targeting zero waste. Currently, there is no widespread and successful standard for industrial seaweed biorefinery design. Polysaccharides have been identified as the most common potential product from Chlorophyta (mainly Ulva spp.), accounting for 40% of the applications. Protein was second (21%), with lipids and pigments considered less frequently (Joniver etal. 2021). Future steps for the development of an Ulva biorefinery should include the demonstration of using common food and chemical industry methods for processing and equipment that can be scaled. These efforts will require mass and
CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 21 energy balances for each step. The subsequent steps should include process simulation using common industry tools, such as AspenPlus (https://www.aspentech.com/en/products/ engineering/aspen-plus) or SuperPro (https://www.intelligen. com/) process design software, enabling economic and life cycle analysis of processes and plants. Further steps should include an integrated process demonstration for assessing product safety, stability, final applications, and complete economic and environmental analysis. This step will require the collaboration of biomass producers, process engineers, and environmental economists. 7. Patents of Ulva-based products and technologies The diversification of macroalgal applications, including Ulva species, in increasingly sophisticated products, is accelerating the emerging macroalgal biotechnology patent market. The rate of patent registrations for seaweed-related products has been steadily increasing annually by approximately 11% (Mazarrasa etal. 2014). Similarly, increased Ulva production and demand for natural products have promoted research and development in Ulva biotechnology. Consequently, patents for processes and applications of Ulva have rapidly grown. Since 2014, 405 Ulva-related patents have been registered, representing 5.4% of seaweed-related registered patents (Mazarrasa et al. 2014). A more recent search using the keyword “Ulva” on the European Patent Office (EPO) website (https://www.epo.org/searching-for- patents.html) resulted in 2,954 patents related to Ulva-based products, which are classified under nine different codes according to the International Patent Classification (IPC) System (Supplementary Table 2). Of the classified patents, Ulva-related patents are distributed into categories relating to medicine (31%), cosmetics (31%), feed (19%) and modifications of nutritive qualities of food and dietic products (10%), revealing that Ulva-related patents in the food industry are lagging behind the medicine, cosmetics and feed industries. 8. Future research directions Several technical and environmental challenges must be overcome to fully capture and realize the potential of Ulva biomass in the European circular economy. In fact, this is one of the main goals of the recently established COST Action CA20106 SeaWheat, which has resulted in the establishment of the network of authors who have collaborated on this manuscript. For successful large-scale production of Ulva spp. for the food, feed, and biomaterials industry, several challenges must be overcome through research, innovation, knowledge transfer and collaboration. Green seaweed species misidentification inhibits production data analysis, making a thorough overview of national and global productions difficult. Ulva species must be correctly identified owing to their popular application in commercial projects and industrial product labeling. Consequently, an integrative systematics approach is required to accurately identify Ulva spp., considering morphological characters, DNA sequencing of different markers, and species biogeography. Such scientific advances will contribute to a better understanding of the Ulva biomass produced, allowing the development of a management plan and policy framework adapted to the specificity of this species’ clades. Nevertheless, it is unrealistic to expect that existing and future producers of Ulva biomass will have the time and resources to double-check the identity of their product using genetic sequencing methods. In order for the Ulva-based industry in Europe to grow, new methods need to be developed that simplify this task, such as the sequencing-free assay for foliose Ulva species identification developed by Fort et al. (2021). Such technological advances will provide quicker and cheaper tools that will enable producers to guarantee the identity of the products they are selling. Likewise, not all Ulva strains and species with economic potential have been identified, and further research into fine-tuned selection for specific applications is required. Additionally, population, strain, and environment-induced chemical variations complicate the development of chemically consistent biomass, which is key for developing an industry striving for nutritionally valuable ingredients or bioactive components for high-end uses. Correct identification of Ulva spp. would also contribute to a better understanding of the effect of genetic and environmental parameters on their composition, growth, and reproduction in their natural and controlled environment. Future research must therefore focus on harnessing the benefits of both genetic and environmental factors in order to support growth of the Ulva cultivation industry. This includes identifying robust strains (e.g., green tide strains Fort, et al. (2020)) with exceptional growth rates and/or high temperature tolerance, and optimizing the cultivation conditions in order to produce biomass with the desired traits (e.g., high proteins or high lipids). Future monitoring and selection programs are necessary to support these efforts and provide food and feed manufacturers with high quality biomass. As a first step toward closing these knowledge gaps, the SeaWheat COST Action has initiated a European-wide collection campaign to measure the nutritional content and microbiome of genetically barcoded Ulva species throughout Europe using standardized methods. These data will provide the first coordinated, European-wide effort to assess the species diversity and the assosiated biochemical and nutritional profiles and epibiontic microbial interactions of Ulva spp. throughout Europe. Additionally, the effect of associated microbiota on Ulva must be further investigated. The close association between bacteria and the development and morphology of Ulva biomass has been demonstrated; however, further interactions within the seaweed holobiont could provide clues for manipulating desired traits in the seaweed. For example, current research by the authors is showing that protoplast development in Ulva spp. can occur naturally. While we do not yet know what triggers the natural production of protoplasts, if we could induce the production by manipulating the microbiome or other environmental factors, then this would provide a cheap and simple method to vegetatively produce large amounts of biomass, without relying on the expensive
22 L. C. HOFMANN ETAL. enzymes that are currently required to induce protoplast development in Ulva spp. Sustainable algal biomass production should include safe approaches, ensuring no harm to natural environments and ecosystems, including wild seaweed populations. Recently, three major challenges were identified for the expansion of seaweed cultivation in temperate environments: global climate change, limited carrying capacity in areas where large-scale cultivation already occurs, and the increasing cost and age of the seaweed labor force (Rieve, 2023). In order to overcome these challenges, the availability and suitability of areas for sea-based cultivation must be accounted for in marine spatial planning and form a beneficial component in coastal conservation, though restrictions on infrastructure may occur. The land-based cultivation approaches must be energy- and cost-efficient, based on full life-cycle assessment and implementation. Furthermore, significant investments must be made in the preservation of seaweed strains for preserving biodiversity, strain selection and selective breeding campaigns for the development of robust strains. Several initiatives have begun to support these efforts among European (SeaStrains), American (SugarKelpBase) global (Global Seaweed Coalition), and Asian networks. The general principles and requirements of seaweed food safety in the EU are subject to the EU-enforced Regulation (EC) number 852/2004 on food hygiene. In many countries, the food manufacturing process is subject to the HACCP assessment, a system adopted by the WHO and the Codex Alimentarius Commission as recommended international code of practice for general principles of food hygiene. The regulation (EC) 68/2013 defines the use of algae as accepted feed materials. Green seaweeds are solely mentioned in the case of seaweed meals. No specific mentions are made for Ulva species. Whether offered live or processed (chilled, frozen, or dried), the compulsory declarations are the contents of crude protein, crude fat, crude ash, and iodine, which should be <100 ppm. However, considering the new market trends and processing technologies of seaweed feed and food products, guidelines and legislation on specific seaweed feed and food products remain lacking. Furthermore, whether legislation from one part of the world can be transferred to other areas without considering the biological (seaweed and microbial flora) and environmental (climatic) factors is doubtful. Although societal acceptance of algal products has increased in Europe recently, further progress is needed to replace conventional biomass or nutritional constituent sources with plant and algae-based ingredients. Clear regulations on quality control relating to environmental contaminants, such as heavy metals and potential pathogens, must be implemented while ensuring the satisfaction of regulatory bodies, consumer safety, and medium- and large-scale practicability for industries. Quality control of strain/biomass origin and chemical composition must be assured based on standardized methodologies. Currently, the European Committee for Electrotechnical Standardization (CEN) is developing standards for algae and algae-based products, representing a major step toward realizing this potential. EU regulatory bodies, including EFSA, must review current restrictions on algae-derived products to support the effective integration of Ulva (or other seaweed) utilization in the European circular economy. Therefore, the risks related to feed and food safety and the possible environmental contamination from aquaculture, among other potential sources of pollution, represent important issues that require special attention from scientists and policymakers concerning the safe use of Ulva spp. in food and feed products. Ulva species produced in land-based systems under a controlled environment would present easily manageable Table 5. Ulva biorefinery. Co-production of various ingredients from Ulva and their transformation to additional products. species directly co-extracted products Products produced by transformation of Ulva-derived ingredients reference U. lactuca water-soluble proteins and carbohydrates (Postma et al. 2018) U. lactuca Protein and carbohydrates Glucose, rhamnose and xylose, acetone, butanol, ethanol, and 1,2-propanediol (Bikker et al. 2016) U. fasciata Mineral rich liquid extract, lipid, ulvan, and cellulose ethanol (trivedi etal., 2015) U. lactuca Mineral rich liquid, lipid, ulvan, protein, and cellulose (Gajaria etal., 2017) U. lactuca water-soluble carbohydrates acetone, butanol, and ethanol (aBe) (van der wal etal., 2013) U. rigida Carbohydrate, salt, concentrated protein (Pezoa-Conte etal., 2015) U. ohnoi salt, pigment, ulvan, and protein (Glasson etal., 2017) U. lactuca Mineral rich liquid extract, ulvan, protein Methane (Mhatre etal., 2019) U. ohnoi salts, starch, lipids, ulvan, proteins, and cellulose. (Prabhu etal., 2019) Mix of U. rigida and U. fascia Hydrochar, 5-HMF, monosaccharides, proteins, peptides. ethanol (Polikovsky etal. 2020) U. ohnoi Mixture of monosaccharides ethanol (Jiang etal., 2016) U. ohnoi starch, proteins, and minerals (Prabhu etal., 2019) U. ohnoi Hydrochar Polyhydroxyalkanoates (Ghosh etal., 2021) U. lactuca Polysaccharides, proteins (andrade et al. 2022) Mix of ulva species Monosaccharides (robin etal., 2017) Ulva sp. not defined Polysaccharides Biodiesel (ruangrit et al., 2023) U. ohnoi Hydrochar, monosaccharides Polyhydroxyalkanoates (steinbruch etal., 2020) U. lactuca antioxidants and phenolic compounds (rashad et al. 2023) Ulva sp. not defined ulvan Biogas, polyhydroxyalkanoates (arul Manikandan and lens 2023) Ulva rigida and Ulva ohnoi water-soluble and -insoluble protein (robin etal., 2018) U. lactuca Bio-oil, hydrochar Bioethanol (sharmiladevi, swetha, and Gopinath 2023)
CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 23 food and feed safety risks. The EU has also listed organic regulations (Council Regulation 834/2007) that classify farmed or wild-collected seaweeds, including Ulva species, as organic. However, when produced under IMTA, more data and scientific-based evidence would be needed relating to the risk posed by the production of low-level trophic organisms using different waste streams and processes. Such information would also help in developing the lacking regulations appropriate for IMTA products. Further, the wild-harvested biomass should be closely monitored because heavy metals, associated pathogens, and other persistent environmental or anthropogenic pollutants can pose risks stemming from seaweed consumption. Using Ulva spp. and its derivative bioactive compounds in feed and food can be challenging as many of the compound’s bioactivity remains unrecognized. Furthermore, high polysaccharide content and non-protein nitrogen are problematic and reduce digestibility. Non-starch polysaccharides (e.g., ulvan) also trap about 5% of the amino acid in the biomass. Solutions such as fermentation to improve digestibility, extended fresh water washing to reduce ash content, and biorefinery approaches for producing bioactive extracts for feed additives have all shown promising results. Nevertheless, further research is required to provide supportive and applicable information regarding the factors determining the presence and level of ANFs in the biomass, their active mechanism, the threshold level at which they are harmful, and methods for neutralizing their activity. Such research will contribute to defining the safe yet bioactive level of inclusion of Ulva ingredients in feed and food formulation. Further, when used as food or feed ingredients, the interactions between Ulva or its derivative ingredients with the matrix should be researched to ensure its safe utilization or conservation of the bioactive characteristics in the formulated feed or food. Furthermore, studies addressing the effect of culinary treatments on the levels of contaminants and bioavailability of health-promoting compounds are also needed. The major challenge that currently hinders the widespread integration of Ulva into feed and food is competition with soybean. As presented above, differences in lipid and protein content separate the nutritional profile of Ulva most strongly from soy. Soybean has about 36.5% protein (USDA FoodData Central), compared to harvested Ulva, which ranges from about 4–27%. Only enriched Ulva grown with supplemental nitrogen can reach protein levels comparable to soybean. Additionally, the cost of Ulva production cannot currently compete with the cheap production of soybean. According to the US Department of Agriculture, soybean production costs about $162/acre. Assuming an average yield of 50 bushels/acre and a conversion rate of 40 bushels/ton, soybean production on a weight basis is approximately $130/ton. In comparison, estimates of production costs for seaweed farms range from $225 – $10,000/ dry ton, depending on scale (Kite-Powell et al. 2022). Therefore, even the largest seaweed farm with the lowest production costs is still 1.7 times more expensive to produce than soybean, and most seaweed farms have even higher production costs. Unfortunately, there are no known published production costs for Ulva cultivation, but life cycle assessments of land-based production are currently underway. Another major limitation for integrating Ulva into the feed industry, both terrestrial and aquafeed, is the scale of production. Currently, the scale of Ulva production is catering mainly to human consumption, while biomass from green tides is used for animal feed research. Clearly it is important to save high quality biomass from aquaculture for human food, and the feed and biomaterials industries should not compete with human food for Ulva biomass, but the unpredictability of the availability of biomass from year to year continues to be a difficult challenge for industries relying on wild biomass. In both the food and feed industries, digestibility, taste, palatability, and flavors must be investigated further to better understand the potential attractiveness of Ulva products to animals or consumers. Customer acceptance and willingness to pay must be examined to determine the marketability and price of Ulva-based products. Currently, some producers are approaching well-known chefs to include seaweeds in their recipes, or to provide cooking courses. Such activities will help raise awareness about how to use seaweeds in general and Ulva specifically in food, and make European consumers more comfortable with incorporating Ulva into their diet. Although Ulva is naturally available and culture techniques exist, several key issues exist regarding the market, technology, and product development (i.e., increased supply of Ulva biomass, product innovation, and processing). The effects of processing on chemical composition and potential modifications in bioactive profiles must be identified by companies and adjusted for end-user applications. To capitalize on the potential for increased profitability, the existing Ulva sector must migrate into the identified opportunity areas. The nutraceutical, pharmaceutical, and cosmetics industries represent greater profit opportunities than the agri-products and horticultural products sector alone (Barbier et al. 2019). To achieve this, the sector must identify specific market opportunities, innovate, and introduce greater automation, including new processing and packaging technology. Effective Ulva biomass utilization in a cascading biorefinery concept will still need to demonstrate its potential to avoid compound loss and waste. Because improving crude biomass often requires high energy investments, the cost-effectiveness and environmental sustainability of such processes must be investigated. Life cycle assessment of current production systems will provide key insights into the sustainability and cost-effectiveness of Ulva production. Therefore, the Ulva industry has been assigned an ambitious target. Greater value in the Ulva sector can only be achieved by industry activities in association with funding agencies and research providers. Acknowledgements The authors would like to thank the European Cooperation in Science and Technology (COST) for making this work possible, as well as two anonymous reviewers whose constructive comments greatly improved the manuscript.
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