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Review

Invasive Seaweeds in the Iberian Peninsula: A Contribution for Food Supply

by
Diana Pacheco
1,
Glacio Souza Araújo
2,
João Cotas
1,
Rui Gaspar
1,
João M. Neto
1 and
Leonel Pereira
1,*
1
Department of Life Sciences, Marine and Environmental Sciences Centre (MARE), University of Coimbra, 3000-456 Coimbra, Portugal
2
Federal Institute of Education, Science and Technology of Ceará–IFCE, Campus Aracati, CE 040, km 137,1, Aracati 62800-000, Ceará, Brazil
*
Author to whom correspondence should be addressed.
Mar. Drugs 2020, 18(11), 560; https://doi.org/10.3390/md18110560
Submission received: 23 October 2020 / Revised: 6 November 2020 / Accepted: 12 November 2020 / Published: 16 November 2020
(This article belongs to the Special Issue Characterization of Bioactive Components in Edible Algae II)
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Abstract

:
The introduction of exotic organisms in marine ecosystems can lead to economic and ecological losses. Globally, seaweeds represent a significant part of these non-indigenous species (NIS), with 407 introduced algal species. Furthermore, the presence of NIS seaweeds has been reported as a major concern worldwide since the patterns of their potential invasion mechanisms and vectors are not yet fully understood. Currently, in the Iberian Peninsula, around 50 NIS seaweeds have been recorded. Some of these are also considered invasive due to their overgrowth characteristic and competition with other species. However, invasive seaweeds are suitable for industrial applications due to their high feedstock. Hence, seaweeds’ historical use in daily food diet, allied to research findings, showed that macroalgae are a source of nutrients and bioactive compounds with nutraceutical properties. The main goal of this review is to evaluate the records of NIS seaweeds in the Iberian Peninsula and critically analyze the potential of invasive seaweeds application in the food industry.

1. Introduction

Seaweeds’ ecological relevance has been acknowledged by the scientific community through the assessment of the ecosystem services they provide, which directly or indirectly support human well-being, namely regulating, provisioning, and cultural services [1,2].
Algae play a pivotal regulatory role in the aquatic environment, being sources of primary and secondary production, providing protection to coastal zones, and as nursery areas [3]. Moreover, seaweeds are a food source for many aquatic organisms, supporting provisioning services for a wide range of invertebrates [4]. Furthermore, seaweeds are part of cultural heritage and distinctiveness in each area, presenting economic value for society [5].
However, these ecosystems are currently under threat due to climatic changes, such as ocean acidification or the increasing seawater temperature [6]. Despite that, anthropogenic pollution nodes are major stressors that affect the structure and functioning of aquatic environments. For instance, eutrophication is a phenomenon provoked by the discharge of effluents with a high inorganic load (i.e., phosphorus, nitrogen, nitrate, nitrite) that can lead to eutrophication. Thus, the excess of nutrients will lead to the occurrence of algal blooms, giving an advantage to opportunistic algae that will affect the structure of the community and its primary productivity [7]. Regarding the available resources, non-indigenous species (NIS) usually are more effective when using them than native species [8]. However, NIS presence can have negative, positive, or neutral effects on the ecosystems where they are integrated [9]. Still, the introduction of exotic species in marine ecosystems can often lead to severe changes in ecosystem functioning. Among the vectors which favored the introduction of exotic seaweeds related to marine traffic rising [10] are, namely, through the discharge of ballast waters and biofouling on recreational boats or cargo ships hulls [11,12,13]. Another possible introduction vector is associated with the aquaculture, importation, and commercialization of marine organisms, namely mollusks [14]. Moreover, it is still found exotic and/or invasive species commercially available in the European aquarium trade markets, such as Caulerpa racemosa and Caulerpa taxifolia [15].
Whenever exotic seaweed species are introduced in a different geographic area and if the biotic and abiotic conditions allow it, these species can exhibit an invasive behavior. Moreover, a set of characteristics are needed to consider it an invasive seaweed species, commonly related to opportunistic traits such, such as a fast growth rate, dynamic life cycle, high recruitment rate, physiology, size, and fitness [3,16,17,18]. However, the intrinsic mechanisms associated with the biologic invasion’s success are not yet fully understood due to their complexity [3]. For these reasons, macroalgal marine invaders are considered a threat to coastal and estuarine environments.
The Iberian Peninsula macroalgal community has also been a target of the introduction of several exotic seaweed species (Table 1), in which some of them are well established, exhibiting a widespread distribution in this area and invasive behavior.
Against this scenario, it urges the need to mitigate the impacts of seaweeds invasions in coastal and estuarine ecosystems, prioritizing the mapping of exotic seaweed species and comprehend the mechanisms which allow the success or failure of the invasion in order to take control and conservation measures [17,28,29].
Among the several adaptative advantages of invasive seaweeds, their high growth rate makes them suitable to feedstock supply for industrial exploitation. Thus, the goal of this review is to critically analyze the potential of invasive seaweeds’ direct or indirect application in the food industry.

2. Invasive Seaweeds: An Important Feedstock to Food Industry

2.1. Red Seaweeds

In marine ecosystems, seaweeds that belong to the phylum Rhodophyta constitute a wide taxonomic diversity [30]. Among the exotic seaweeds registered on the Iberian Peninsula, Pyropia suborbiculata (Kjellman) (J.E. Sutherland, H.G. Choi, M.S. Hwang and W.A. Nelson 2011 it is an Asiatic Bangiales), due to its high tolerance to the variation of physico-chemical conditions, is now widespread throughout the American, Australian, and European shoreline [31,32,33]. However, the first records of P. suborbiculata in the Atlantic Ocean were misidentified with Neopyropia yezoensis M.S. Hwang and H.G. Choi (formerly Pyropia yezoensis) [34]. Through molecular analysis, in 2005, it was possible to genetically distinguish these two seaweed species [35]. More recently, researchers found that P. suborbiculata is well established on the Iberian Peninsula and is genetically similar to the population from the Pacific Ocean, suggesting that the presence of this exotic seaweed in the Northwest Atlantic is probably through marine shipping [31,36]. In contrast, P. suborbiculata is produced through aquaculture and is authorized and considered safe for human consumption in the United States of America [37,38]. In fact, this seaweed can have a significant role in the daily diet (Figure 1) and can be used fresh or dried, milled, and then utilized as a flavor enhancer [39].
However, it is in the Asiatic region that this seaweed currently assumes a high economic interest, being considered an important marine crop for food feedstock [40,41]. In these countries, seaweeds which belongs to Pyropia/Porphyra/Neopyropia genus are highly consumed by the population [42]. Therefore, P. suborbiculata is also a potential candidate for food industry feedstock due to its protein (11.2% DW), lipids (0.3% DW), and carbohydrates (31.6% DW) content [43].
The health benefits that this food resource presents, lead to increased customer demand, which allowed a sales volume increase and the global economic expansion of Pyropia/Porphyra commercialization [44].
Thus, Pyropia/Porphyra/Neopyropia spp. farming became essential to guarantee the feedstock. However, these cultivations are frequently affected by fungal diseases. For instance, the fungi Pythium porphyrae provokes the most concerning disease (red rot disease) in Asiatic Pyropia aquacultures [45,46], causing seaweed blades destruction, precluding the entire cultivation, and leading to serious economic losses [47]. Nevertheless, studies showed that P. suborbiculata is more resistant to P. porphyrae fungal attack [48], thus being a potential candidate for food supply through their cultivation.
Another introduced red seaweed native from Japan, Agarophyton vermiculophyllum (Ohmi) Gurgel, J.N. Norris et Fredericq 2018 (previously known as Gracilaria vermiculophylla) (Figure 2), has invaded estuaries throughout the whole world. Although the presence of this algae was underrated in several areas due to the morphological similarity with native species Gracilaria gracilis [49], many signs of progress have been made through genetic analysis in order to distinguish them [50,51].
In Europe, some authors defend that this seaweed was unintentionally introduced through Japanese oysters farming, migrating birds, or shipping [50]. Since then, this species is well established in the Iberian Peninsula because they can tolerate abiotic parameters variation such as temperature (11–25 °C) and salinity (10–30 PSU) [50]. Due to this species resilience, they are recognized by their environmental and ecological impact on fauna and flora [4,52,53].
From a nutritional perspective, A. vermiculophyllum is rich in monounsaturated and polyunsaturated fatty acids (22.2 mg/kg DW and 4 mg/kg DW, respectively) [54]. They also have interesting phosphorus (0.082–0.203%) and nitrogen (2.27–4.68%) content [55].
For this reason, this seaweed already had shown to be a low-cost tool to supplement animal feed to improve aquaculture fish nutritional profile and their organoleptic quality. For instance, researchers found out that adding only 5% of A. vermiculophyllum on rainbow trout feed increase fish iodine levels and improve fillet color and texture [56].
However, this agarophyte seaweed also indirectly contributes to the food industry. Agar is a phycocolloid highly valuable for this sector. In this red seaweed, agar content can reach up to 30% of their dry weight [57] and it could be incorporated in food products as gelling, stabilizing, and encapsulating agent due to its rheological properties [58,59]. Furthermore, agar biofilm enriched with A. vermiculophyllum extract can be used in edible fruits and vegetables, maintaining properties such as color and light gloss up [58].
More recently, aiming for plastic waste reduction, A. vermiculophyllum was used to develop sustainable fish packaging [60]. In this study, the extracts from this seaweed were applied to allow the antimicrobial activity of the fish packaging [60] Furthermore, seaweeds can contribute to innovation in the food sector while contributing to food security [61].
Grateloupia turuturu Yamada 1941 (Figure 3) shows a resilient behavior, presenting a high reproduction rate and tolerating a wide range of temperatures (4–29 °C) and salinity (22–37 PSU), thus threatening several native seaweeds [62]. Therefore, this seaweed native from Japan currently exhibits a cosmopolitan distributional pattern [14]. However, until 2002, the taxonomic identification of G. turuturu was misidentified with Grateloupia doryphora (Montagne), whereas a research group was able to distinguish them through molecular techniques [63]. Hence, the first occurrence of this seaweed in Europe was in 1982 and was observed in the Iberian Peninsula in the early 1990s [64]. The authors hypothesize that this species was introduced through their biofouling capacity on hulls or oyster shells [14].
Despite the records of the direct consumption of G. turuturu in Asian countries [65], the full nutraceutical potential of this seaweed is still unrevealed in Europe. However, some researchers are focused on their chemical composition and their bioactivities. G. turuturu is an edible seaweed that already contributes to food demand due to their protein (22% DW), lipid (2% DW), dietary (60% DW), insoluble fibers (12% DW), and sterols content [65,66,67,68]. It is also important to highlight the concentration of phycoerythrin (0.30% DW) and phycocyanin (0.033% DW) [67]. Besides that, this macroalgae is also a source of essential amino acids such as histidine (1.8 g protein-N), leucine (6.3 g protein-N), tryptophan (0.7 g protein-N), lysine (4.3 g protein–N), methionine (2 g protein-N), phenylalanine (3.7 g protein-N), threonine (3 g protein-N), and valine (4.9 g protein-N) [66,69].
Researchers evaluated the nutritional profile of this red seaweed in Portugal [70] (Table 2) and demonstrated that the most abundant macronutrients are sodium (Na) and potassium (K), exhibiting 96.08 and 20 mg/g DW, respectively. While magnesium (Mg), calcium (Ca), and phosphorus (P) were found at a concentration ranging 2–2.81 mg/g DW. Regarding the micronutrient concentration, most representatives were zinc (Zn) and iron (Fe), while the other trace elements analyzed presented a vestigial concentration (Table 3).
In fact, the daily intake of these elements is extremely important to the human body and guarantees good metabolic functions [71]. For instance, a study conducted by Pang et al. (2006) [72] with G. turuturu collected in China showed that this edible red seaweed can be a human health promoter through their antibacterial activity against Vibrio parahaemolyticus.
The red seaweed Asparagopsis armata Harvey 1855 (Figure 4), native from Australia, was intentionally introduced in Europe due to the high food demand in 1920 [78,79,80]. Then, this seaweed species was maintained by aquaculture in Ireland [79], which lead to their dispersion through this country.
Some authors hypothesize that the introduction of exotic seaweed in the Iberian Peninsula was associated with oyster transportation and commercialization [81,82]. Since then, this seaweed species has been well established in the Northwest coast of the Iberian Peninsula [83].
There are records that this species has been used as food [84]. In fact, A. armata is rich in several micronutrients (Table 3) that are essential in lower concentrations to the good function of the human body, such as calcium (4.47% DW), sodium (9.36% DW), magnesium (1.38% DW), and phosphorus (0.27% DW). However, this seaweed is also rich in trace elements that are important in lower concentrations to human health, namely zinc (66.3 mg/kg), copper (13 mg/kg), manganese (62.3 mg/kg), and iron (1188 mg/kg) [70,77]. Moreover, A. armata contains a high protein content that can reach 18.3% DW, with the synthesis of essential amino acids, such as isoleucine, valine, lysine, methionine, phenylalanine, histidine, and tryptophan, which the human metabolism is not able to synthesize [85].
Besides that, the chemical composition of this seaweed presents several interesting bioactive compounds with applications in the food industry. In the Portuguese coast, researchers found that sterols represent 555 mg/kg A. armata dry weight namely, desmosterol, fucosterol, and b-sitosterol [86,87], which are anti-cholesterol compounds [87,88]. Moreover, this red alga also contains halogenated metabolites, such as bromine, chlorine, and iodine-containing methane, ethane, ethanol, acetaldehyde, acetone, 2-acetoxypropane, propene, epoxypropane, acrolein, and butenone [89,90,91,92], which are bioactive molecules with antifungal, antimicrobial and antibiotic effects [90,93,94].
Hence, the direct consumption of this seaweed, even in lower quantities, can be considered a supplement to the human daily diet. However, many studies have currently been focused on the incorporation of A. armata as an animal feed supplement in order to improve meat quality and reduce methane emissions [95].
Asparagopsis taxiformis (Delile) Trevisan 1845 (Figure 5) is a red seaweed native from Australia [96], with a high capability to cope with temperature variations [97], thus being distributed through tropic and sub-tropical regions [98]. This species is currently well established in Europe and is considered an invasive seaweed species in the Iberian Peninsula, particularly in Spain and in the Portuguese archipelagos (Azores and Madeira), due to their coverage area and noxious effects on the surrounding fauna and flora [74,98,99].
Among other seaweeds, there are historical records in Hawaii of A. taxiformis usage as a nutraceutical food due to their lipids, proteins, and carbohydrates (Table 2) content [100]. Further studies corroborated the ethnobotanical application of this seaweed in the Hawaiian daily diet, revealing the biochemical composition of this seaweed.
In the Portuguese islands, the biomass of this seaweed was also analyzed in order to evaluate its nutritional profile, revealing to be a good source of macronutrients [73]. For this reason, many recipes including A. taxiformis were developed, such as soups, salads, or scrambled eggs [101].
Asparagopsis taxiformis presents a rich composition in micronutrients and trace elements (Table 3). For instance, Selmi et al. (2020) [76] evaluated A. taxiformis nutritional profile of biomass harvested from Tunisia, which revealed a high content in iron (0.2189 mg/g), sodium (0.200 mg/g), and potassium (0.13784 mg/g), which are pivotal micronutrients to the good function of osmoregulatory processes in the human body. Meanwhile, the trace element with more representativity in A. taxiformis biomass was manganese, with a concentration of 3.05 × 10−3 mg/g. However, the other elements, namely, arsenic, cadmium, copper, mercury, and lead, demonstrated to be present in concentrations lower than 5 × 10−4 mg/g.
This seaweed also presents nutraceutical potential as an iodine supplier, presenting a concentration up to 3.37 g/100g DW, benefiting people who suffer from a deficit of this micronutrient [102,103].
In summary, the invasive seaweeds from the Iberian Peninsula analyzed exhibit a rich nutritional composition in macro and micronutrients that are pivotal to complement a human health diet, even in low amounts (Table 3). However, it is necessary to consider that seaweed nutritional profiles vary according to the species, geographical place, tidal exposure, season, physico-chemical composition of the water, or even with the seaweed processing techniques [104]. Regarding the direct seaweed application in the food industry, consumers hold a concern relatively to metal concentration. Table 3 shows the nutrient value reference (NVR) according to the European Food Safety Authority (EFSA) [105]. Researchers analyzed A. taxiformis content in warning pollutants, namely As (4 × 10−4 mg/g DW), Cd (2 × 10−5 mg/g DW), Hg (2 × 10−5 mg/g DW), and Pb (5.1 × 10−4 mg/g DW), revealing lower concentrations relative to the NVR for each element [106,107,108,109,110].

2.2. Brown Seaweeds

Colpomenia peregrina Sauvageau 1927 (Figure 6) is a brown seaweed native from the Northwest Pacific [111]. This species is characterized for being annual, with globular physiology and for being extremely tolerant to environmental conditions variation, such as salinity (15–30 PSU) and temperature (13–20 °C) [112,113]. For this reason, C. peregrina is such a cosmopolitan species with ease in establishing in new areas. However, this exotic species can be easily misidentified with a native Portuguese seaweed, Colpomenia sinuosa. Thus, C. peregrina is characterized by the thinness of the thallus, hairs arising from the sub-cortical cells not associated with the sori, which are confluent, not punctate, and have no pellicle over the plurilocular sporangia, which are shorter than those of C. sinuosa [114].
This exotic seaweed was firstly observed in Cadiz (Spain) in 1806 [115] and nowadays is present in the European temperate regions, including the Northwest of the Iberian Peninsula [116]. Researchers hypothesize that the introduction of this NIS could have occurred through the coastal cultivation of oysters in France. This seaweed grows attached to the oyster shells and when C. peregrina bladder fills up with air and water, is transported through the oceanic streams [116,117].
Despite the widespread distribution of C. peregrina, there are just a few studies regarding their nutritional profile and biomass valorization. Nevertheless, a group of researchers harvested this species in Southwest England in the United Kingdom (U.K.) and determined that the composition of C. peregrina is mostly minerals, representing 85.3% of this seaweed dry weight, in which 12.2% DW are carbohydrates, 2.48% DW protein, and 0.8% DW lipids [118]. Further analysis was performed in order to evaluate their micronutrient profile (Table 4).
According to the available data, the high K and P content (46.93 and 0.67 mg/g, respectively) indicates that this seaweed can be a potential biomass feedstock for the agriculture industry as a natural fertilizer. Regarding as a food source, C. peregrina is valuable due to its Ca content (55.64 mg/g), which can be beneficial for people who suffer from diseases related to calcium deficit, such as osteoporosis [119].
Despite the high silicon content (252.29 mg/g) [118], it was estimated that a daily dietary intake of 20–50 mg silicon/day by an average adult with 60 kg is unlikely to cause health problems [120]. Nevertheless, it is necessary to consider that the aluminum concentration found in C. peregrina exceeds the tolerable upper intake recommended by EFSA.
Sargassum muticum (Yendo) Fensholt 1955 (Figure 7) is a native seaweed from Japan and China, being currently widespread along the European shoreline. Due to their high tolerance to hydrodynamic, temperature, and solar exposure variations, this species possess a huge ability to acclimatize and maintenance in different areas with distinct climate conditions [121,122]. Hence, their fast reproduction and growth rate makes them thrive after their introduction, assuming an invasive character [123,124].
These Japanese-native seaweed species was inadvertently introduced into European Atlantic waters in the early 1970s. The first record of S. muticum in Europe was in the English Channel [125] and quickly spread to the Iberian Peninsula [126,127,128]. It is necessary to consider that the presence of this seaweed in marine ecosystems causes a serious macroalgal biodiversity loss due to the shading they produce, blocking the sunlight to other native species [129,130,131]. The authors theorize that the introduction of S. muticum in the Iberian Peninsula was probably due to oysters for aquaculture or through the spread of spores during transport of ballast water and its discharge [131].
Seaweeds chemical characterization mostly reflects the abiotic and biotic conditions where they grow, so according to the harvesting area, S. muticum biomass will present variations in the nutritional profile, namely in the macronutrients (Table 5), micronutrients, and trace elements (Table 6).
In general, S. muticum nutritional profile from India, whereas the fresh biomass was analyzed, is notably lower than the macroalgal biomass collected in the other countries.
Comparatively, with the biomass collected in Spain, S. muticum harvested in the U.K. presented higher carbohydrates and ash content, which could possibly be related to the chemical composition presented in the marine ecosystem. In contrast, the lipid concentration of the biomass harvested in the U.K. and Spain exhibited a similar value. For instance, S. muticum collected in Spain had a variation between 20.10% and 31.77% of total fatty acids content, whereas polyunsaturated fatty acids composition during the year presents a balanced ω-6/ω-3 ratio (1.40–3.37) [133], which is the recommended ratio for human food consumption by the World Health Organization (WHO) and as reviewed by Leandro et al., 2020 [61].
The overall biochemical analysis also shows that S. muticum contains a high concentration of carbohydrates, mostly alginic acid, which has a behavior of dietary fiber in the human gastric system.
However, it is also necessary to consider that the chemical composition of the macroalgal biomass varies within the biotic and abiotic parameters fluctuation in each sampling site [43]. Besides that, the drying process (time and temperature) can interfere with the nutritional yield and further valorization [133].
The nutrient richness of this seaweed species is highlighted in Table 6. Even though seaweed species are well-known metal bioaccumulators, the metal content analyzed in the biomass harvested in Spain exhibits metal concentrations below the threshold defined by EFSA [105,108,120].
Regarding the differences observed within the countries analyzed, is necessary to consider that seaweeds’ chemical composition can be affected by several factors, such as the nutrient’s availability, pollution nodes, and other environmental parameters related to the geographical zone where the biomass is harvested [134,135]. However, this can only be corroborated with previous physico-chemical characterization of the habitat.
Although S. muticum has been already exploited for aquaculture production in China [136] and it is a traditional food in Korea [137], there is no commercial use of this biomass for food consumption in Europe nor in rest of the non-native location [138].
S. muticum contribution as an value-added product has been reviewed by Milledge, Nielsen, and Bailey (2016), highlighting the application as food, feed, and biofertilizers to agriculture crops [139].
Silva et al. (2019) [140] analyzed the effects of aqueous extracts of S. muticum as seed germination enhancer and as plant biofertilizer in two commercial sub-variants of Lactuca sativa (Lettuce) [140]. However, the germination assay proved that a high seaweed extract concentration inhibits seed germination. Nevertheless, the concentration of 25% was the best concentration for seed germination. In the biofertilizer assay, the same extract concentration (25%) demonstrated to be the most effective treatment. The S. muticum extract treatment revealed also that the plants were able to assimilate a higher minerals content, mainly P, K, Ca, Mg from the soil. These results show that S. muticum treatment can have an efficient multirole effect in the agricultural crop.
Regarding the animal feed industry, S. muticum can also contribute as a feed supplement to the holothurian and abalone aquaculture cultivation [141].
Undaria pinnatifida (Harvey) Suringar 1873 (Figure 8) is annual kelp, native from the Northeast Pacific, being present in the shoreline of different countries such as Japan, China, Korea, and Oriental Russia. This species can stand a wide range of environmental conditions, such as temperatures from 0–27 °C and salinities as low as 20 PSU [142]. For this reason, this species is nowadays well established in several locations, namely, in the Atlantic, Mediterranean Sea, Pacific Oceania, and Atlantic America coastline, from Argentina to the United States of America [143].
Undaria pinnatifida was first registered in European shoreline in France in 1971 [144]. A probable introduction vector of this Asiatic species into the Iberian Peninsula can be related to the transportation of Pacific oysters, in resemblance with other exotic seaweed species [145]. The two other possible vectors responsible for the introduction of U. pinnatifida are mainly considered to be by boats (mainly trans-Atlantic boats, with cargo boats being one of the best examples for the accidental introduction of NIS); however, accidental introduction by aquaculture is also very well documented, mainly in 18 and 19 centuries [146,147]. Their ecological impact on native fauna and flora is even more concerning than other exotic seaweed species, considering that this is an annual species [148,149].
However, the harvesting and exploitation of this seaweed for direct food consumption, mainly in the Asiatic countries, already control U. pinnatifida biomass and is a sustainable way to mitigate the ecological disturbances caused by their presence in the ecosystems [150].
In Spain, U. pinnatifida is collected and afterward is usually dried in order to be sold for direct consumption [151] or as an ingredient in pre-cooked meals [152]. So, this invasive species cannot be cultivated in non-native habitats but can be harvested from coastal areas and incorporated into the daily human diet, direct or indirectly. Due to the high exploitation of this edible seaweed worldwide, the information available regarding the food nutritional values is very extensive, unlike the other exotic seaweeds analyzed. It is shown how the macronutrients (Table 7), micronutrients, and trace elements (Table 8) concentration varies according to the harvesting site.
According to the literature, U. pinnatifida nutritional profile does not suffer many fluctuations between geographical zones, presenting identical results regarding lipids, proteins, carbohydrates, fibers, and mineral content. However, the lipid and protein profile could be different or exhibit different concentrations of each compound [153,155]. Moreover, U. pinnatifida synthesizes essential amino acids such as histidine, isoleucine, lysine, valine, phenylalanine, and methionine, but in different concentrations according to the geographical region [153,155]. Furthermore, U. pinnatifida from both sites also demonstrated low variations in their macronutrient concentration.
From another perspective, the micronutrient and trace metals concentration are directly affected according to the geographical harvesting zone (Table 8). According to Taboada et al. (2013) and Kolb et al. (2004) [153,155], U. pinnatifida revealed similar contents of potassium in both geographical areas (Japan and Spain). Comparatively, U. pinnatifida biomass harvested in the native zone presented a higher content on calcium and sodium, while the biomass harvested from the Northwest Iberian Peninsula contained higher concentrations of phosphorus and magnesium.
The biomass collected in the invasive place showed a higher concentration in all the presented trace elements, except for nickel and chromium, for which the authors did not present information regarding the concentration of these trace metals in U. pinnatifida from Spain.
Researchers performed the analysis of the iodine (I) content in commercial samples from Europe and from Japan, whereas the European samples revealed a higher I concentration [156]. Thus, the recommended daily intake dose will be different, according to the origin of the seaweed [61].
It is proven that food consumption behavior can modify the skeletal muscle mass and performance. Extracts from the brown seaweed U. pinnatifida were tested on mice as a potential candidate to develop a product to promote muscle mass and functioning [157]. These extracts enhanced the mitochondrial biogenesis, which consequently increased the oxidative muscle fiber in mice and stimulated the angiogenesis in skeletal muscles. Thus, enhanced the mice’s exercise capacity and skeletal muscle mass. The observed effects were derived from the presence of fucoxanthin, hesperetin, and caffeic acid and other bioactive molecules detected in U. pinnatifida extracts.
Undaria pinnatifida fatty acids demonstrated antioxidant and antibacterial activity, which can be used in the food industry [158]. Moreover, several studies have been focused on the application of bioactive compounds extracted from this brown seaweed, such as pigments or polysaccharides as flavor enhancers and to improve the organoleptic properties of food products [135,159].
However, this seaweed can also contribute indirectly to the food industry through crop culture. In fact, this seaweed was already tested as a soil amendment in poor quality soils in tomato production. The results obtained benefited the soil properties and promoted a multirole action as a soil fertilizing agent and enriching the plant with phytohormones and vitamins [160].

2.3. Green Seaweeds

The green seaweed Caulerpa racemosa Forsskål) J. Agardh 1873 (Figure 9) is native from Australia [161]. The presence of this seaweed leads to a significant biodiversity loss, especially in invertebrate diversity and abundance [161]. This seaweed inhabits tropical and warm-temperate regions but tolerates low temperatures down to 10 °C, being a resilient species that easily adapts to variations of biotic and abiotic parameters [161]. For this reason, C. racemosa has currently a widespread distribution throughout the world [162,163,164]. In Spain, the existence of the invading C. racemosa in Alicante, at a depth of 0 to 2 m, was reported [165]. There are several hypotheses to this seaweed species introduction in the Iberian Peninsula, namely, the unintentional introduction through ballast waters and sediment, ship hull fouling, or the through the trade of aquarium species [161].
There are records of the use of C. racemosa in the Indo-Pacific region, where it is appreciated due to the taste, texture, and health-promoting bioactivities [166]. In fact, this species contains an interesting macronutrient composition, namely, in protein (0.6–18.3% DW), carbohydrates (3.6–83.2% DW), lipids (0.1–3.8 8% DW), moisture (8.8–91.5% FW), and ash (14.5–55.1% DW) [167,168,169].
Moreover, C. racemosa contains a micronutrient and trace elements (Table 9) profile based on iron 29.71%, sodium 10.64%, zinc 6.82%, potassium 5.03%, manganese 4.91%, calcium 4.76%, magnesium 1.61%, copper 0.62%, molybdenum 0.15%, and selenium 0.13% [170].
Fractions of sulfated polysaccharides isolated from the extract of the C. racemosa of the coast of Gujrat (India) were analyzed for sugar content and galactose, glucose, arabinose, and xylose were found as the main components [171]. The macroalgae have, among other purposes, the presence of polysaccharides with anti-herpetic activities according to the authors. In addition, they have anti-nociceptive and anti-inflammatory activities [172]. Recently, Reference [173] reported that silver nanoparticles mediated by the macroalga C. racemosa showed excellent antibacterial activities against human pathogenic bacteria Staphylococcus aureus and Proteus mirabilis. In one study, the antioxidant and phenolic content of C. racemosa was higher than red seaweeds [174].
The macroalgae Caulerpa taxifolia (M. Vahl) C. Agardh (1817), native from the tropical and subtropical region of Australia, specifically in Moreton Bay, Southern Queensland, and Lord Howe Island [175], was the first macrophyte invasion to attract public attention. Consequently, authorities in some Mediterranean countries, such as Spain and France, tried to eradicate and control this invasion [144]. According to the authors, the two Caulerpa species were introduced and can co-occur in certain areas of the Mediterranean Sea, such as in Italy, France, Croatia, and Spain. In terms of biomass, C. taxifolia is more prominent than C. racemosa [176].
Thibaut, Meinesz, and Coquillard (2004) clearly showed that one of the main characteristics of the C. taxifolia macroalgae is its perennial life cycle, with relatively high biomass values throughout the year, in different biotopes, which may be a factor in the broad ecological impact of this species on the aquatic environment [177].
This macroalga can present up to 13% of toxic metabolites, which makes its consumption by herbivorous organisms unpleasant [178,179].
For instance, caulerpenyne is the main secondary metabolite produced by C. taxifolia and it plays an important role in the chemical defense of algae [178,179,180]. The presence of this invasive species reduces the availability of microhabitat for fish, resulting in a decrease in species richness, density, and biomass when compared to native communities that live in beds or rocky areas [181]. This metabolite has several biological activities, mainly antitumor activities inhibiting the growth of several cancer cell lines [182]
Codium fragile ssp. fragile (Suringar) Hariot 1889 is apparently originated in the Pacific Ocean, more specifically from the coast of Japan [183], and is one of the most invasive species in the world, having spread from its native range in the NW Pacific to the NE and SE Pacific, N Atlantic, Mediterranean, and the coasts of South Africa, Australia, and New Zealand [184,185].
Once established, C. fragile subsp. fragile grows rapidly and has an inhibitory effect on the recruitment and growth of kelps [186,187]. This resulted in the replacement of Laminaria beds by C. fragile meadows in the Gulf of Maine and along the Atlantic coast of New Scotia [188].
Watanabe, Targets, and Scheibling (2009) [189] cited that the wide variety of propagules are produced by C. fragile and the variable distances over which different types of propagules can be transported give this species the advantage of short- and long-distance dispersion, and probably played a role in the invasive success of this alga in various aquatic environments [189]. This macroalga can be limited by nitrogen availability and its growth and propagation is related to the concentration of nutrients in seawater (for example, eutrophication and resurgence events) [184]
Regarding the fatty acid content, researchers analyzed six species of Codium in southwestern Australia and found that for the native C. fragile alga, the largest amount was of hexadecanoic acid (16:0), 40.50%, followed by oleic acid (18:1ω9), 23.30%, linolenic acid (18:3ω3), 5.60%, and myristic acid (14: 0), 5.30%, also presenting 21.10% of lipids [190]. Herbreteau et al. (1997) [191] collected this macroalga on the Sillon Bay, Cotes d’Amor, France, and obtained yields of decanoic acid (10:0) 48.60%, hexadecanoic acid (16:0) 19.70%, octadecatrienoic acid (18:3) 12.20%, and octadecenoic acid (18:1) 6.20% [191].
Regarding the sulfated polysaccharides in C. fragile collected on the coast of PuTian, China, extracting for 3 h at 115 °CS obtained a yield of 2.10%. In addition, they obtained yields of 30.9% of total sugar, 4.05% of uronic acid, 39.7% of sulfate, and 282 kDa of molecular weight [192].
Rojo et al. (2014) [193] observed that on the Cantabrian coast, northwestern Spain, the invasive C. fragile matured in a smaller size and that this could confer competitive advantages over the native species of the habitat.
To the west of the Iberian Peninsula, in Spain, [29] the effectiveness of marine protection in containing the invasion of six marine macroalgae was evaluated, including Codium fragile, and it was found that the presence of this species was determined by the interaction between exposure and protection, indicating significantly greater biomass in locations outside Marine Protection Areas (MPAs) compared to those within the MPAs. The authors cite that the protection provided by MPAs is very limited to prevent the establishment and spread of the most abundant invasive macroalgae in the aquatic environment and that stricter management plans must be implemented to ensure the resilience of the native ecosystem within MPAs.

3. Pharmacological Potential of the Invasive Seaweeds

Seaweeds are currently considered a wide source of natural compounds with pharmacological potential [139,194,195,196]. In fact, Porphyra/ Pyropia/Neopyropia spp. was used hundreds of years ago as a food and pharmaceutical source in Asian countries [197]. Moreover, Pyropia/Porphyra/Neopyropia spp. are known to contain compounds such as porphyran (a sulfated carbohydrate), mycosporine-like amino acids, and phycoerythrin (a phycobiliprotein) with high applicability in the pharmaceutical industry, exhibiting antioxidant [198,199,200], antihypertensive [201,202], anti-inflammatory [203], anticancer [204,205], anticoagulant [199,206], and immunomodulatory [207,208,209,210] bioactivities.
The agarophyte A. vermiculophyllum can be, as well, a useful tool in the pharmaceutical industry [211]. Besides agar application in molecular biology techniques and microbiology, the activity of agar as a drug delivery agent has been investigated [212,213]. A recent investigation highlighted the potential of hyaluronic acid-agar-based hydrogels in drug delivery in cases of intravitreal treatments [214].
Aside from their nutritional and nutraceutical properties, G. turuturu demonstrated to be a source of bioactive compounds with a pharmaceutical application, namely, R-phycoerythrin [215,216]. Moreover, researchers also tested the antibacterial activity of G. turuturu harvested in Portugal and they observed that these seaweed polysaccharides at a concentration of 15 mg/mL can significantly inhibit the growth of Staphylococcus aureus (88.5%) and Escherichia coli (85.4%) [217].
Both A. armata and A. taxiformis have already confirmed to be a pool of bioactive compounds with pharmacological applications. Researchers demonstrated that a concentration of 1 mg/mL of A. armata dichloromethane extracts was able to significantly reduce Human colorectal cancer model (Caco‑2 cells) proliferation, proving antitumoral bioactivity [218]. For another perspective, A. taxiformis extracts at a concentration of 40 µg/mL exhibited activity against the protozoan Leishmania infantum, which affects animals and humans [219]. Therefore, this red seaweed extract also demonstrated to be efficient in the inhibition of fungal growth, namely, Aspergillus fumigatus, Aspergillus terreus, and Aspergillus flavus [220]. Moreover, these seaweed sulfated polysaccharides were found to be antioxidant and non-cytotoxic to HeLa cells [221]. Furthermore, a study revealed that A. taxiformis aqueous extract, even in low concentration (1.5%), reveals an antiviral effect on crop plants production due to its phytohormones content, such as cytokinins and auxins [222].
Moreover, the polysaccharide fucogalactoglucan extracted from C. peregrina was characterized and its composition revealed to be mainly glucose (50.00–52.91%), galactose (25.5–26.94%), and fucose (20.62–24.56%) [223]. In the same study, its bioactivity was evaluated, demonstrating low cytotoxicity against HeLa cancer cells (< 40%). Besides that, fucogalactoglucan induced RAW264.7 murine macrophage cells to release considerable amounts of nitric oxide (NO) [223]. Thus, the polysaccharide isolated from C. peregrina demonstrated to be a possible immunostimulatory agent to improve the human immune system.
Ethanolic extracts of S. muticum have proven to reduce significantly the expression of adipogenic marked genes, related to body weight, fat tissue content, serum cholesterol, and triglyceride levels in mice fed with high-fat diet [224]. This assay can be the support to further investigation into possible anti-obesity treatment. The phenolic content shows an interesting antioxidant and anti-inflammatory activity, which can be useful in the food and pharmaceutical industry [225]. Furthermore, S. muticum extract revealed bioactivities that protect shrimp against mortal diseases, such as Acute Hepatopancreatic Necrosis Disease [226]. Nevertheless, the current main potential industrial exploitation from S. muticum is the alginate extraction; however, in this sector, kelps are preferentially used by the industry due to the higher yields. The alginate extracted from this species can also be used to remove toxic heavy metals from wastewaters or even from organisms in the case of human metals poisoning [227,228,229].
Undaria pinnatifida has also proven to possess pharmacological potential, likewise anticancer and anti-inflammatory, which can explain the high interest of this seaweed in the food industry worldwide [230]. The application of this Asian kelp as a direct food product acts as a prebiotic, enhancing the intestinal microflora, mainly in the quantity of Bifidobacterium longum colony in the human intestine [159].
Regarding the genus Caulerpa, it is important to highlight the compound caulerpin, which is an alkaloid that present antitumor [231,232] and anti-inflammatory [233] bioactivity, thus being a potential source for the development of novel marine drugs. However, there are still more pharmacological applications to be found. For instance, a recent study demonstrates that the development of caulerpin-based fish feed can increase lipid content on fish flesh [234].
Furthermore, sulfated polysaccharides extracted from the green edible seaweed C. fragile has shown antioxidant bioactivity [235].

4. Conclusions

The ecological and economic significance of marine algal invasion is undisputed in the global context; however, this topic has not received as much attention as it deserves. Although substantial evidence supports the fact of marine algal introduction and invasion, the underlying ecological principles need more attention to better explain such invasions.
Marine algal invasions transcend national boundaries, so the problem must be considered an international problem.
Due to the historical practices of seaweed consumption, the exploitation of invasive seaweeds as a feedstock is a win-win paradigm, economically and as a mitigation control of the invasive macroalgal biomass. Hence, invasive seaweed exhibits a rich nutritional profile in proteins, essential amino acids, lipids, carbohydrates, and minerals that even in low amounts, seaweed direct consumption can be a nutraceutical food product. Moreover, seaweeds are a natural pool of unexplored bioactive compounds with a pharmacological or agricultural application, thus contributing to human health promotion.
Nevertheless, commercial exploitation of invasive marine algae should be undertaken, if at all, with great care and with a full understanding of all aspects of the biology and ecological consequences of the new exotic species. Despite that, it is necessary to consider that the seaweeds biochemical profile varies according to several biotic and abiotic factors. In this context, it urges the need to chemically characterize them prior to utilization or commercialization.

Author Contributions

Conceptualization, D.P., R.G., J.M.N., and L.P.; preparation, D.P., G.S.A., J.C., and R.G.; writing—review and editing, D.P., G.S.A., J.C., R.G., J.M.N., and L.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received external funding by the PTDC/BIA-CBI/31144/2017-POCI-01 project -0145-FEDER-031144-MARINE INVADERS, co-financed by the ERDF through POCI (Operational Program Competitiveness and Internationalization) and by the Foundation for Science and Technology (FCT, IP).

Acknowledgments

This work is financed by national funds through FCT-Foundation for Science and Technology, I.P., within the scope of the projects UIDB/04292/2020-MARE-Marine and Environmental Sciences Centre. Diana Pacheco would like to thank PTDC/BIA-CBI/31144/2017-POCI-01 project -0145-FEDER-031144-MARINE INVADERS, co-financed by the ERDF through POCI (Operational Program Competitiveness and Internationalization) and by the Foundation for Science and Technology (FCT, IP). João Cotas would like to thank the European Regional Development Fund through the Interreg Atlantic Area Program, under the project NASPA (EAPA_451/2016).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Smale, D.A.; Burrows, M.T.; Moore, P.; O’Connor, N.; Hawkins, S.J. Threats and knowledge gaps for ecosystem services provided by kelp forests: A northeast Atlantic perspective. Ecol. Evol. 2013, 3, 4016–4038. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. De Groot, R.; Fisher, B.; Christie, M.; Aronson, J.; Braat, L.; Gowdy, J.; Haines-Young, R.; Maltby, E.; Neuville, A.; Polasky, S.; et al. Integrating the ecological and economic dimensions in biodiversity and ecosystem service valuation. In The Economics of Ecosystems and Biodiversity: Ecological and Economic Foundations; Kumar, P. Ed. Routledge: Landon, UK, 2010. [Google Scholar]
  3. Vieira, R.; Pinto, I.S.; Arenas, F. The role of nutrient enrichment in the invasion process in intertidal rock pools. Hydrobiologia 2017, 797, 183–198. [Google Scholar] [CrossRef]
  4. Haram, L.; Sotka, E.; Byers, J. Effects of novel, non-native detritus on decomposition and invertebrate community assemblage. Mar. Ecol. Prog. Ser. 2020, 643, 49–61. [Google Scholar] [CrossRef]
  5. Scharin, H.; Ericsdotter, S.; Elliott, M.; Turner, R.K.; Niiranen, S.; Blenckner, T.; Hyytiäinen, K.; Ahlvik, L.; Ahtiainen, H.; Artell, J.; et al. Processes for the sustainable stewardship of marine environments. Ecol. Econ. 2016, 128, 55–67. [Google Scholar] [CrossRef]
  6. Forster, J.; Radulovich, R. Seaweed and food security. In Seaweed Sustainability; Tiwari, B.K., Troy, D.J., Eds.; Academic Press: Cambridge, MA, USA, 2015; pp. 289–313. ISBN 9780124186972. [Google Scholar]
  7. Lyons, D.A.; Arvanitidis, C.; Blight, A.J.; Chatzinikolaou, E.; Guy-Haim, T.; Kotta, J.; Orav-Kotta, H.; Queirós, A.M.; Rilov, G.; Somerfield, P.J.; et al. Macroalgal blooms alter community structure and primary productivity in marine ecosystems. Glob. Chang. Biol. 2014, 20, 2712–2724. [Google Scholar] [CrossRef]
  8. Abreu, M.H.; Pereira, R.; Sousa-Pinto, I.; Yarish, C. Ecophysiological studies of the non-indigenous species Gracilaria vermiculophylla (Rhodophyta) and its abundance patterns in Ria de Aveiro lagoon, Portugal. Eur. J. Phycol. 2011, 46, 453–464. [Google Scholar] [CrossRef] [Green Version]
  9. William, S.L.; Smith, J.E. A Global Review of the Distribution, Taxonomy, and Impacts of Introduced Seaweeds. Annu. Rev. Ecol. Evol. Syst. 2007, 38, 327–359. [Google Scholar] [CrossRef] [Green Version]
  10. Simard, N.; Pelletier-Rousseau, M.; Clarke Murray, C.; Mckindsey, C.W.; Therriault, T.W.; Lacoursière-rouseel, A.; Bernier, R.; Sephton, D.; Drolet, D.; Locke, A.; et al. National Risk Assessment of Recreational Boating as a Vector for Aquatic Invasive Species; Fisheries and Oceans Canada Canadian Science Advisory Secretariat: Ottawa, ON, Canada, 2017. [Google Scholar]
  11. Mineur, F.; Johnson, M.P.; Maggs, C.A. Macroalgal Introductions by Hull Fouling on Recreational Vessels: Seaweeds and Sailors. Environ. Manag. 2008, 42, 667–676. [Google Scholar] [CrossRef]
  12. Mineur, F.; Johnson, M.P.; Maggs, C.A.; Stegenga, H. Hull fouling on commercial ships as a vector of macroalgal introduction. Mar. Biol. 2007, 151, 1299–1307. [Google Scholar] [CrossRef]
  13. Flagella, M.M.; Verlaque, M.; Soria, A.; Buia, M.C. Macroalgal survival in ballast water tanks. Mar. Pollut. Bull. 2007, 54, 1395–1401. [Google Scholar] [CrossRef]
  14. Hewitt, C.L.; Campbell, M.L.; Schaffelke, B. Introductions of seaweeds: Accidental transfer pathways and mechanisms. Bot. Mar. 2007, 50, 50. [Google Scholar] [CrossRef]
  15. Vranken, S.; Bosch, S.; Peña, V.; Leliaert, F.; Mineur, F.; De Clerck, O. A risk assessment of aquarium trade introductions of seaweed in European waters. Biol. Invasions 2018, 20, 1171–1187. [Google Scholar] [CrossRef] [Green Version]
  16. Van Kleunen, M.; Weber, E.; Fischer, M. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol. Lett. 2010, 13, 235–245. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Hu, Z.-M.; Juan, L.-B. Adaptation mechanisms and ecological consequences of seaweed invasions: A review case of agarophyte Gracilaria vermiculophylla. Biol. Invasions 2014, 16, 967–976. [Google Scholar] [CrossRef]
  18. Murphy, J.T.; Johnson, M.P.; Viard, F. A theoretical examination of environmental effects on the life cycle schedule and range limits of the invasive seaweed Undaria pinnatifida. Biol. Invasions 2017, 19, 691–702. [Google Scholar] [CrossRef] [Green Version]
  19. BOE Real Decreto 630/2013, de 2 de Agosto, por el que se Regula el Catálogo Español de Especies Exóticas Invasoras; BOE-A-2013-8565; Ministerio de Agricultura, Alimentación y Medio Ambiente Español: Madrid, Spain, 2013; Volume 185, pp. 1–21.
  20. Peteiro, C. Macroalgas Alóctonas en la Demarcación Marina Noratlántica de la Costa Española; Informe del Instituto Español de Oceanografía (IEO): Madrid, Spain, 2014. [Google Scholar]
  21. Berecibar, E. Identificação Das Espécies de Macroalgas Não Indígenas da Costa Portuguesa; Projeto BioMar PT. EMEPC: Paço de Arcos, Portugal, 2016; pp. 2–3. [Google Scholar]
  22. Gorostiaga, J.; Santolaria, A.; Secilla, A.; Casares, C.; Díez, I. Check-list of the Basque coast benthic algae (North of Spain). An. Jard. Bot. Madr. 2004, 61, 155–180. [Google Scholar] [CrossRef]
  23. Chainho, P.; Fernandes, A.; Amorim, A.; Ávila, S.P.; Canning-Clode, J.; Castro, J.J.; Costa, A.C.; Costa, J.L.; Cruz, T.; Gollasch, S.; et al. Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands. Estuar. Coast. Shelf Sci. 2015, 167, 199–211. [Google Scholar] [CrossRef]
  24. Berecibar, E. Long-term Changes in the Phytogeography of the Portuguese Continental Coast. Ph.D. Thesis, University of Algarve, Faro, Portugal, 2011. [Google Scholar]
  25. Peña, V.; Bárbara, I.; Grall, J.; Maggs, C.A.; Hall-Spencer, J.M. The diversity of seaweeds on maerl in the NE Atlantic. Mar. Biodivers. 2014, 44, 533–551. [Google Scholar] [CrossRef]
  26. Hu, Z.M.; Fraser, C. Seaweed Phylogeography: Adaptation and Evolution of Seaweeds under Environmental Change; Springer: Dordrecht, The Netherlands, 2016; ISBN 9789401775342. [Google Scholar]
  27. Montes, M.; Rico, J.M.; García-Vazquez, E.; Pichs, Y.J.B. Molecular barcoding confirms the presence of exotic Asian seaweeds (Pachymeniopsis gargiuli and Grateloupia turuturu) in the Cantabrian Sea, Bay of Biscay. PeerJ 2017, 2017. [Google Scholar] [CrossRef] [Green Version]
  28. Valentine, J.P.; Magierowski, R.H.; Johnson, C.R. Mechanisms of invasion: Establishment, spread and persistence of introduced seaweed populations. Bot. Mar. 2007, 50, 50. [Google Scholar] [CrossRef]
  29. Blanco, A.; Lemos, M.F.L.; Pereira, L.; Gaspar, R. Mapping Invasive Macroalgae in the Western Iberian Peninsula: A Methodological Guide; Servizo de publicacións da Universidade de Vigo: Vigo, Spain, 2020; ISBN 9788481588408. [Google Scholar]
  30. Cornish, M.L.; Monagail, M.M.; Critchley, A.T. The Animal Kingdom, Agriculture... and Seaweeds. J. Mar. Sci. Eng. 2020, 8, 574. [Google Scholar] [CrossRef]
  31. Vergés, A.; Sánchez, N.; Peteiro, C.; Polo, L.; Brodie, J.; Vergé, A.S.; Sar Peteiro, C.; Polo, I.; A, V.S. Pyropia suborbiculata (Bangiales, Rhodophyta): First records from the northeastern Atlantic and Mediterranean of this North Pacific species. Phycologia 2013, 52, 121–129. [Google Scholar] [CrossRef]
  32. Sánchez, N.; Vergés, A.; Peteiro, C.; Sutherland, J.E.; Brodie, J. Diversity of bladed Bangiales (Rhodophyta) in Western Mediterranean: Recognition of the genus Themis and descriptions of T. ballesterosii sp. nov., T. iberica sp. nov., and Pyropia parva sp. nov. J. Phycol. 2014, 50, 908–929. [Google Scholar] [CrossRef]
  33. Monotilla, W.D.; Notoya, M. Morphological and physiological responses of Porphyra suborbiculata Kjellman (Bangiales, Rhodophyta) blades from five localities. Bot. Mar. 2004, 47. [Google Scholar] [CrossRef]
  34. Kornmann, P. Porphyra yezoensis bei Helgoland - eine entwicklungsgeschichtliche Studie. Helgol. Meeresunters. 1986, 40, 327–342. [Google Scholar] [CrossRef] [Green Version]
  35. Milstein, D.; Cabral De Oliveira, M. Molecular phylogeny of Bangiales (Rhodophyta) based on small subunit rDNA sequencing: Emphasis on Brazilian Porphyra species. Phycologia 2005, 44, 212–221. [Google Scholar] [CrossRef]
  36. Broom, J.E.; Nelson, W.A.; Yarish, C.; Jones, W.A.; Aguilar Rosas, R.; Aguilar Rosas, L.E. A reassessment of the taxonomic status of Porphyra suborbiculata, Porphyra carolinensis and Porphyra lilliputiana (Bangiales, Rhodophyta) based on molecular and morphological data. Eur. J. Phycol. 2002, 37, S0967026202003566. [Google Scholar] [CrossRef]
  37. USDA; Agricultural Marketing Service; Agricultural Analytics Division. Marine Plants & Algae Organic Production and Handling; USDA National Organic Program: Washington, DC, USA, 2016.
  38. Erhart, S.; Cerier, L. Sea Vegetable Celebration; Book Publishing Company: Summertown TN, 2001. [Google Scholar]
  39. US FDA. CFR–Code of Federal Regulations Title 21; U.S. Food and Drug Administration: Washington, DC, USA, 2018.
  40. Koh, Y.H.; Kim, M.S. Genetic diversity and distribution pattern of economic seaweeds Pyropia yezoensis and Py. suborbiculata (Bangiales, Rhodophyta) in the northwest Pacific. J. Appl. Phycol. 2020, 32, 2495–2504. [Google Scholar] [CrossRef]
  41. Kang, J.W. Species of cultivated Porphyra in Korea. Korean J. Fish. Aquat. Sci. 1970, 3, 77–92. [Google Scholar]
  42. Noda, H. Health benefits and nutritional properties of nori. J. Appl. Phycol. 1993, 5, 255–258. [Google Scholar] [CrossRef]
  43. Kaehler, S.; Kennish, R. Summer and winter comparisons in the nutritional value of marine macroalgae from Hong Kong. Bot. Mar. 1996, 39, 11–17. [Google Scholar] [CrossRef]
  44. Hwang, E.K.; Park, C.S. Seaweed cultivation and utilization of Korea. Algae 2020, 35, 107–121. [Google Scholar] [CrossRef]
  45. Schwelm, A.; Badstöber, J.; Bulman, S.; Desoignies, N.; Etemadi, M.; Falloon, R.E.; Gachon, C.M.M.; Legreve, A.; Lukeš, J.; Merz, U.; et al. Not in your usual Top 10: Protists that infect plants and algae. Mol. Plant Pathol. 2018, 19, 1029–1044. [Google Scholar] [CrossRef]
  46. Hwang, E.K.; Park, C.S.; Kakinuma, M. Physicochemical responses of Pythium porphyrae (Oomycota), the causative organism of red rot disease in Porphyra to acidification. Aquac. Res. 2009, 40, 1777–1784. [Google Scholar] [CrossRef]
  47. Badis, Y.; Han, J.W.; Klochkova, T.A.; Gachon, C.M.M.; Kim, G.H. The gene repertoire of Pythium porphyrae (Oomycota) suggests an adapted plant pathogen tackling red algae. ALGAE 2020, 35, 133–144. [Google Scholar] [CrossRef]
  48. Rodríguez, J.P.; Terrados, J.; Rosenfeld, S.; Méndez, F.; Ojeda, J.; Mansilla, A. Correction to: Effects of temperature and salinity on the reproductive phases of Macrocystis pyrifera (L.) C. Agardh (Phaeophyceae) in the Magellan region. J. Appl. Phycol. 2019, 31, 929. [Google Scholar] [CrossRef] [Green Version]
  49. Byrne, K.; Zuccarello, G.C.; West, J.; Liao, M.-L.; Kraft, G.T. Gracilaria species (Gracilariaceae, Rhodophyta) from southeastern Australia, including a new species, Gracilaria perplexa sp. nov.: Morphology, molecular relationships and agar content. Phycol. Res. 2002, 50, 295–311. [Google Scholar] [CrossRef]
  50. Rueness, J. Life history and molecular sequences of Gracilaria vermiculophylla (Gracilariales, Rhodophyta), a new introduction to European waters. Phycologia 2005, 44, 120–128. [Google Scholar] [CrossRef]
  51. Gurgel, C.F.D.; Norris, J.N.; Schmidt, W.E.; Le, H.N.; Fredericq, S. Systematics of the gracilariales (Rhodophyta) including new subfamilies, tribes, subgenera, and two new genera, Agarophyton gen. nov. and Crassa gen. nov. Phytotaxa 2018, 374, 1–23. [Google Scholar] [CrossRef]
  52. Wallentinus, I.; Nyberg, C.D. Introduced marine organisms as habitat modifiers. Mar. Pollut. Bull. 2007, 55, 323–332. [Google Scholar] [CrossRef] [PubMed]
  53. Nyberg, C.D.; Thomsen, M.S.; Wallentinus, I. Flora and fauna associated with the introduced red alga Gracilaria vermiculophylla. Eur. J. Phycol. 2009, 44, 395–403. [Google Scholar] [CrossRef]
  54. Santos, S.A.O.; Vilela, C.; Freire, C.S.R.; Abreu, M.H.; Rocha, S.M.; Silvestre, A.J.D. Chlorophyta and Rhodophyta macroalgae: A source of health promoting phytochemicals. Food Chem. 2015, 183, 122–128. [Google Scholar] [CrossRef] [PubMed]
  55. Bermejo, R.; MacMonagail, M.; Heesch, S.; Mendes, A.; Edwards, M.; Fenton, O.; Knöller, K.; Daly, E.; Morrison, L. The arrival of a red invasive seaweed to a nutrient over-enriched estuary increases the spatial extent of macroalgal blooms. Mar. Environ. Res. 2020, 158, 104944. [Google Scholar] [CrossRef] [PubMed]
  56. Valente, L.M.P.; Rema, P.; Ferraro, V.; Pintado, M.; Sousa-Pinto, I.; Cunha, L.M.; Oliveira, M.B.; Araújo, M. Iodine enrichment of rainbow trout flesh by dietary supplementation with the red seaweed Gracilaria vermiculophylla. Aquaculture 2015, 446, 132–139. [Google Scholar] [CrossRef]
  57. Kumar, S.; Gupta, R.; Kumar, G.; Sahoo, D.; Kuhad, R.C. Bioethanol production from Gracilaria verrucosa, a red alga, in a biorefinery approach. Bioresour. Technol. 2013, 135, 150–156. [Google Scholar] [CrossRef]
  58. Sousa, A.M.M.; Sereno, A.M.; Hilliou, L.; Gonçalves, M.P. Biodegradable agar extracted from Gracilaria vermiculophylla: Film properties and application to edible coating. Mater. Sci. Forum 2010, 636–637, 739–744. [Google Scholar] [CrossRef]
  59. Phan, T.D.; Debeaufort, F.; Luu, D.; Voilley, A. Functional Properties of Edible Agar-Based and Starch-Based Films for Food Quality Preservation. J. Agric. Food Chem. 2005, 53, 973–981. [Google Scholar] [CrossRef]
  60. Baek, S.K.; Song, K. Bin Development of Gracilaria vermiculophylla extract films containing zinc oxide nanoparticles and their application in smoked salmon packaging. LWT Food Sci. Technol. 2018, 89, 269–275. [Google Scholar] [CrossRef]
  61. Leandro, A.; Pacheco, D.; Cotas, J.; Marques, J.C.; Pereira, L.; Gonçalves, A.M.M.M. Seaweed’s Bioactive Candidate Compounds to Food Industry and Global Food Security. Life 2020, 10, 140. [Google Scholar] [CrossRef]
  62. Simon, C.; Ar Gall, E.; Deslades, E. Expansion of the red alga Grateloupia doryphora along the coasts of Brittany (France). Hydrobiologia 2001, 443, 23–29. [Google Scholar] [CrossRef]
  63. Gavio, B.; Fredericq, S. Grateloupia turuturu (Halymeniaceae, Rhodophyta) is the correct name of the non-native species in the Atlantic known as Grateloupia doryphora. Eur. J. Phycol. 2002, 37, 349–359. [Google Scholar] [CrossRef] [Green Version]
  64. Pérez-cirera, J.L.; Cremades, J.; Bárbara, I. Grateloupia lanceola (Cryptonem¡ales, Rhodophyta) en las costas de la Península Ibérica: Estudio morfológico y anatómico. Biologia (Bratisl). 1989, 134, 123–134. [Google Scholar]
  65. Levring, T.; Hoppe H., A.; Schmid O., J. Marinae Algae, A Survey of Research and Utilization. Fette, Seifen, Anstrichm. 1969, 71, 1020. [Google Scholar] [CrossRef]
  66. Fujiwara-Arasaki, T.; Mino, N.; Kuroda, M. The protein value in human nutrition of edible marine algae in Japan. In Eleventh International Seaweed Symposium; Springer: Dordrecht, The Netherlands, 1984; pp. 513–516. [Google Scholar]
  67. Denis, C.; Morançais, M.; Li, M.; Deniaud, E.; Gaudin, P.; Wielgosz-Collin, G.; Barnathan, G.; Jaouen, P.; Fleurence, J. Study of the chemical composition of edible red macroalgae Grateloupia turuturu from Brittany (France). Food Chem. 2010, 119, 913–917. [Google Scholar] [CrossRef]
  68. Kendel, M.; Couzinet-Mossion, A.; Viau, M.; Fleurence, J.; Barnathan, G.; Wielgosz-Collin, G. Seasonal composition of lipids, fatty acids, and sterols in the edible red alga Grateloupia turuturu. J. Appl. Phycol. 2013, 25, 425–432. [Google Scholar] [CrossRef]
  69. Munier, M.; Dumay, J.; Morançais, M.; Jaouen, P.; Fleurence, J. Variation in the biochemical composition of the edible seaweed Grateloupia turuturu Yamada harvested from two sampling sites on the brittany coast (France): The influence of storage method on the extraction of the seaweed pigment r-phycoerythrin. J. Chem. 2013, 2013, 1–8. [Google Scholar] [CrossRef] [Green Version]
  70. Rodrigues, D.; Freitas, A.C.; Pereira, L.; Rocha-Santos, T.A.P.; Vasconcelos, M.W.; Roriz, M.; Rodríguez-Alcalá, L.M.; Gomes, A.M.P.; Duarte, A.C. Chemical composition of red, brown and green macroalgae from Buarcos bay in Central West Coast of Portugal. Food Chem. 2015, 183, 197–207. [Google Scholar] [CrossRef]
  71. Pereira, L. A review of the nutrient composition of selected edible seaweeds. In Seaweed: Ecology, Nutrient Composition and Medicinal Uses; Pomin, V.H., Ed.; Nova Science Publishers, Inc.: Hauppauge, NY, USA, 2011; pp. 15–47. ISBN 978-1-61470-878-0. [Google Scholar]
  72. Pang, S.J.; Xiao, T.; Shan, T.F.; Wang, Z.F.; Gao, S.Q. Evidences of the intertidal red alga Grateloupia turuturu in turning Vibrio parahaemolyticus into non-culturable state in the presence of light. Aquaculture 2006, 260, 369–374. [Google Scholar] [CrossRef]
  73. McDermid, K.J.; Stuercke, B. Nutritional composition of edible Hawaiian seaweeds. J. Appl. Phycol. 2003, 15, 513–524. [Google Scholar] [CrossRef]
  74. Nunes, N.; Ferraz, S.; Valente, S.; Barreto, M.C.; Pinheiro de Carvalho, M.A.A. Biochemical composition, nutritional value, and antioxidant properties of seven seaweed species from the Madeira Archipelago. J. Appl. Phycol. 2017, 29, 2427–2437. [Google Scholar] [CrossRef]
  75. El-Baroty, G.S.; Moussa, M.Y.; Shallan, M.; Ali, M.; Sabh, Z.; Shalaby, E. Department Contribution to the Aroma, Biological Activities, Minerals, Protein, Pigments and Lipid Contents of the Red Alga: Asparagopsis taxiformis (Delile) Trevisan. J. Appl. Sci. Res. 2007, 3, 1825–1834. [Google Scholar]
  76. Selmi, A.; Khiari, R.; Snoussi, A.; Bouzouita, N. Analysis of Minerals and Heavy Metals Using ICP-OES and FTIR Techniques in Two Red Seaweeds (Gymnogongrus griffithsiae and Asparagopsis taxiformis) from Tunisia. Biol. Trace Elem. Res. 2020. [Google Scholar] [CrossRef] [PubMed]
  77. Roque, B.M.; Salwen, J.K.; Kinley, R.; Kebreab, E. Inclusion of Asparagopsis armata in lactating dairy cows’ diet reduces enteric methane emission by over 50 percent. J. Clean. Prod. 2019, 234, 132–138. [Google Scholar] [CrossRef]
  78. Horridge, G.A. Occurrence of Asparagopsis armata Harv. on the scilly Isles. Nature 1951, 167, 732–733. [Google Scholar] [CrossRef]
  79. Kraan, S.; Barrington, K.A. Commercial farming of Asparagopsis armata (Bonnemaisoniceae, Rhodophyta) in Ireland, maintenance of an introduced species? J. Appl. Phycol. 2005, 17, 103–110. [Google Scholar] [CrossRef]
  80. Monagail, M.M.; Morrison, L. The seaweed resources of Ireland: A twenty-first century perspective. J. Appl. Phycol. 2020, 1–14. [Google Scholar] [CrossRef]
  81. Vaz-Pinto, F.; Olabarria, C.; Arenas, F. Propagule pressure and functional diversity: Interactive effects on a macroalgal invasion process. Mar. Ecol. Prog. Ser. 2012, 471, 51–60. [Google Scholar] [CrossRef]
  82. Trowbridge, C.D. A global proliferation of non-native marine and brackish macroalgae. In World Seaweed Resources—An Authoritative Reference System; Critchley, A.T., Ohno, M., Largo, D.B., Eds.; ETI Bioinformatics: Amsterdam, The Netherlands, 2006. [Google Scholar]
  83. Blanco, A.; Neto, J.M.; Troncoso, J.; Lemos, M.F.L.; Olabarria, C. Effectiveness of two western Iberian Peninsula marine protected areas in reducing the risk of macroalgae invasion. Ecol. Indic. 2020, 108, 105705. [Google Scholar] [CrossRef]
  84. Zahmatkesh, F.; Gaspar, R.; Pereira, L. Marine Invasive Seaweeds of the Iberian Peninsula for Value Added Products. In Encyclopedia of Marine Biotechnology; Wiley: Hoboken, NJ, USA, 2020; p. 3248. ISBN 0263034612001. [Google Scholar]
  85. Pellegrini, M.; Pharo, P.; Sciences, F. Contribution ä etude chimique des Algues Mediterraneennes. Bot. Mar. 1967, 12, 9–14. [Google Scholar]
  86. Lopes, G.; Sousa, C.; Bernardo, J.; Andrade, P.B.; Valentão, P.; Ferreres, F.; Mouga, T. Sterol profiles in 18 macroalgae of the portuguese coast. J. Phycol. 2011, 47, 1210–1218. [Google Scholar] [CrossRef] [PubMed]
  87. El Hattab, N.; Daghbouche, Y.; El Hattab, M.; Piovetti, L.; Garrigues, S.; De La Guardia, M. FTIR-determination of sterols from the red alga Asparagopsis armata: Comparative studies with HPLC. Talanta 2006, 68, 1230–1235. [Google Scholar] [CrossRef] [PubMed]
  88. Brufau, G.; Canela, M.A.; Rafecas, M. Phytosterols: Physiologic and metabolic aspects related to cholesterol-lowering properties. Nutr. Res. 2008, 28, 217–225. [Google Scholar] [CrossRef] [PubMed]
  89. Woolard, F.X.; Moore, R.E.; Roller, P.P. Halogenated acetic and acrylic acids from the red alga Asparagopsis taxiformis. Phytochemistry 1979, 18, 617–620. [Google Scholar] [CrossRef]
  90. McConnell, O.; Fenical, W. Halogen chemistry of the red alga Asparagopsis. Phytochemistry 1977, 16, 367–374. [Google Scholar] [CrossRef]
  91. Burreson, B.J.; Moore, R.E.; Roller, P.P. Volatile Halogen Compounds in the Alga Asparagopsis taxiformis (Rhodophyta). J. Agric. Food Chem. 1976, 24, 856–861. [Google Scholar] [CrossRef]
  92. Paul, N.A.; De Nys, R.; Steinberg, P.D. Chemical defence against bacteria in the red alga Asparagopsis armata: Linking structure with function. Mar. Ecol. Prog. Ser. 2006, 306, 87–101. [Google Scholar] [CrossRef] [Green Version]
  93. Genovese, G.; Tedone, L.; Hamann, M.T.; Morabito, M. The Mediterranean red alga Asparagopsis: A source of compounds against Leishmania. Mar. Drugs 2009, 7, 361–366. [Google Scholar] [CrossRef] [Green Version]
  94. Salvador, N.; Gómez Garreta, A.; Lavelli, L.; Ribera, M.A. Antimicrobial activity of Iberian macroalgae. Sci. Mar. 2007, 71, 101–113. [Google Scholar] [CrossRef] [Green Version]
  95. Kinley, R.D.; Martinez-Fernandez, G.; Matthews, M.K.; de Nys, R.; Magnusson, M.; Tomkins, N.W. Mitigating the carbon footprint and improving productivity of ruminant livestock agriculture using a red seaweed. J. Clean. Prod. 2020, 259, 120836. [Google Scholar] [CrossRef]
  96. Andreakis, N.; Costello, P.; Zanolla, M.; Saunders, G.W.; Mata, L. Endemic or introduced? Phylogeography of Asparagopsis (Florideophyceae) in Australia reveals multiple introductions and a new mitochondrial lineage. J. Phycol. 2016, 52, 141–147. [Google Scholar] [CrossRef] [PubMed]
  97. Martins, G.M.; Cacabelos, E.; Faria, J.; Álvaro, N.; Prestes, A.C.L.; Neto, A.I. Patterns of distribution of the invasive alga Asparagopsis armata Harvey: A multi-scaled approach. Aquat. Invasions 2019, 14, 582–593. [Google Scholar] [CrossRef]
  98. Ní Chualáin, F.; Maggs, C.A.; Saunders, G.W.; Guiry, M.D. The invasive genus Asparagopsis (Bonnemaisoniaceae, Rhodophyta): Molecular systematics, morphology, and ecophysiology of Falkenbergia isolates. J. Phycol. 2004, 40, 1112–1126. [Google Scholar] [CrossRef]
  99. Cacabelos, E.; Martins, G.M.; Faria, J.; Prestes, A.C.L.; Costa, T.; Moreu, I.; Neto, A.I. Limited effects of marine protected areas on the distribution of invasive species, despite positive effects on diversity in shallow-water marine communities. Biol. Invasions 2020, 22, 1169–1179. [Google Scholar] [CrossRef]
  100. Abbott, I.A. Limu. An Ethnobotanical Study of Some Hawaiian Seaweeds; National Tropical Botanical Garden: Kauai, HI, USA, 1996. [Google Scholar]
  101. Unidade de Bioquímica, M. Seaweed Recipes. Available online: http://www.ubqmadeira.com/category/receitas/ (accessed on 3 September 2020).
  102. Nunes, N.; Valente, S.; Ferraz, S.; Barreto, M.C.; Pinheiro de Carvalho, M.A.A. Nutraceutical potential of Asparagopsis taxiformis (Delile) Trevisan extracts and assessment of a downstream purification strategy. Heliyon 2018, 4. [Google Scholar] [CrossRef] [Green Version]
  103. Ferraz, S. Different Seaweeds Use for Iodine Deficiency Overcome. Biomed. J. Sci. Tech. Res. 2019, 15, 13–16. [Google Scholar] [CrossRef]
  104. Rupérez, P. Mineral content of edible marine seaweeds. Food Chem. 2002, 79, 23–26. [Google Scholar] [CrossRef]
  105. EFSA Overview on Tolerable Upper Intake Levels as derived by the Scientific Committee on Food (SCF) and the EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA). Eur. Food Saf. Auth. 2018, 3, 4.
  106. EFSA Scientific Opinion on Lead in Food. EFSA J. 2010, 8, 1–151. [CrossRef]
  107. Alexander, J.; Benford, D.; Cockburn, A.; Cravedi, J.; Dogliotti, E.; Di Domenico, A.; Fernández-cruz, M.L.; Fink-gremmels, J.; Fürst, P.; Galli, C.; et al. Cadmium in food, scientific opinion of the Panel on Contaminants in the food chain. EFSA J. 2009, 1019, 1–76. [Google Scholar]
  108. EFSA Scientific Opinion on Arsenic in Food. EFSA J. 2009, 7, 1351. [CrossRef]
  109. Panel, E.; Chain, F. Scientific Opinion on the risk for public health related to the presence of mercury and methylmercury in food. EFSA J. 2012, 10. [Google Scholar] [CrossRef]
  110. Aguilar, F.; Autrup, H.; Barlow, S.; Castle, L.; Crebelli, R.; Dekant, W.; Gontard, N.; Gott, D.; Grilli, S.; Leclercq, C.; et al. Safety of aluminium from dietary intake - Scientific Opinion of the Panel on Food Additives, Flavourings, Processing Aids and Food Contact Materials (AFC). EFSA J. 2008, 6, 1–34. [Google Scholar] [CrossRef]
  111. Abbott, I.A.; Isabella, A.; Hollenberg, G.J. Marine Algae of California; Stanford University Press: Palo Alto, CA, USA, 1992. [Google Scholar]
  112. Lee, K.M.; Boo, G.H.; Coyer, J.A.; Nelson, W.A.; Miller, K.A.; Boo, S.M. Distribution patterns and introduction pathways of the cosmopolitan brown alga Colpomenia peregrina using mt cox3 and atp6 sequences. J. Appl. Phycol. 2014, 26, 491–504. [Google Scholar] [CrossRef]
  113. Pereira, L. Seaweed flora of the European North Atlantic and Mediterranean. In Handbook of Marine Biotechnology; Kim, S.K., Ed.; Springer: Berlin/Heidelberg, Germany, 2015; pp. 65–178. [Google Scholar]
  114. Fatemeh, Z. Sampling, Mapping and Adding Value to Marine Invasive Seaweeds of the Iberian Peninsula. Master’s Thesis, University of Coimbra, Coimbra, Portugal, 2017. [Google Scholar]
  115. Blackler, H. The occurrence of Colpomenia peregrina (Sauv.) Hamel in the Mediterranean (Phaeophyta, Scytosiphonales). Blumea 1967, 15, 5–8. [Google Scholar]
  116. Green, L.A.; Mathieson, A.C.; Neefus, C.D.; Traggis, H.M.; Dawes, C.J. Southern expansion of the brown alga Colpomenia peregrina Sauvageau (Scytosiphonales) in the Northwest Atlantic Ocean. Bot. Mar. 2012, 55, 643–647. [Google Scholar] [CrossRef] [Green Version]
  117. Minchin, A. Further distributional records of the adventive marine brown alga Colpomenia peregrina (Phaeophyta) in Ireland. Irish Nat. J. 1991, 23, 380–381. [Google Scholar]
  118. Beacham, T.A.; Cole, I.S.; DeDross, L.S.; Raikova, S.; Chuck, C.J.; Macdonald, J.; Herrera, L.; Ali, T.; Airs, R.L.; Landels, A.; et al. Analysis of seaweeds from South West England as a biorefinery feedstock. Appl. Sci. 2019, 9, 4456. [Google Scholar] [CrossRef] [Green Version]
  119. Allen, L.; de Benoist, B.; Dary, O.; Hurrel, R. Guidelines on Food Fortification with Micronutrientes; World Health Organization: Geneva, Switzerland, 2006. [Google Scholar]
  120. Zhou, J.; Chen, X. Tolerable upper intake level on vitamins and minerals. J. Hyg. Res. 2004, 33, 771–773. [Google Scholar]
  121. Tanniou, A.; Vandanjon, L.; Gonçalves, O.; Kervarec, N.; Stiger-Pouvreau, V. Rapid geographical differentiation of the European spread brown macroalga Sargassum muticum using HRMAS NMR and Fourier-Transform Infrared spectroscopy. Talanta 2015, 132, 451–456. [Google Scholar] [CrossRef]
  122. Kraan, S. Sargassum muticum (Yendo) Fensholt in Ireland: An invasive species on the move. J. Appl. Phycol. 2008, 20, 825–832. [Google Scholar] [CrossRef]
  123. Álvarez-Canali, D.; Sangil, C.; Sansón, M. Fertile drifting individuals of the invasive alien Sargassum muticum (Fucales, Phaeophyceae) reach the coasts of the Canary Islands (eastern Atlantic Ocean). Aquat. Bot. 2020, 103322. [Google Scholar] [CrossRef]
  124. Harries, D.; Cook, E.; Donnan, D.; Mair, J.; Harrow, S.; Wilson, J. The establishment of the invasive alga Sargassum muticum on the west coast of Scotland: Rapid northwards spread and identification of potential new areas for colonisation. Aquat. Invasions 2007, 2, 367–377. [Google Scholar] [CrossRef]
  125. Farnham, W.F.; Fletcher, R.L.; Irvine, L.M. Attached Sargassum found in Britain. Nature 1973, 243, 2. [Google Scholar] [CrossRef]
  126. Critchley, A.T.; Farnham, W.F.; Morrell, S.L. A chronology of new European sites of attachment for the invasive brownalga, Sargassum muticum, 1973–1981. J. Mar. Biol. Assoc. UK 1983, 63, 799–811. [Google Scholar] [CrossRef]
  127. Rueness, J. Sargassum muticum and other introduced Japanese macroalgae: Biological pollution of European coasts. Mar. Pollut. Bull. 1989, 20, 173–176. [Google Scholar] [CrossRef]
  128. Fernández, C. Ecology of Sargassum muticum (Phaeophyta) on the north coast of Spain: IV. Sequence of colonization on ashore. Bot. Mar. 1999, 42, 553–562. [Google Scholar] [CrossRef]
  129. Anadón, R.; Fernández, C. Comparación de tres comunidades de horizontes intermareales con abundancia de Gelidium latifolium (Grev.) Born et Thur. en la costa de Asturias (N. de España). Inv. Pesq. 1986, 50, 353–366. [Google Scholar]
  130. Sanchez, I.; Fernandez, C.; Arrontes, J. Long-term changes in the structure of intertidal assemblages after invasion by Sargassum muticum (Phaeophyta). J. Phycol. 2005, 41, 942–949. [Google Scholar] [CrossRef]
  131. Critchley, A.T.; Farnham, W.F.; Yoshida, T.; Norton, T.A. A bibliography of the invasive alga Sargassum muticum (Yendo) Fensholt (Fucales; Sargassaceae). Bot. Mar. 1990, 33, 551–562. [Google Scholar] [CrossRef]
  132. Fouda, W.A.; Ibrahim, W.M.; Ellamie, A.M.; Ramadan, G. Biochemical and mineral compositions of six brown seaweeds collected from red sea at hurghada coast. Indian J. Geo-Marine Sci. 2019, 48, 484–491. [Google Scholar]
  133. Balboa, E.M.; Gallego-Fábrega, C.; Moure, A.; Domínguez, H. Study of the seasonal variation on proximate composition of oven-dried Sargassum muticum biomass collected in Vigo Ria, Spain. J. Appl. Phycol. 2016, 28, 1943–1953. [Google Scholar] [CrossRef]
  134. Kumar, M.S.; Sharma, S.A. Toxicological effects of marine seaweeds: A cautious insight for human consumption. Crit. Rev. Food Sci. Nutr. 2020, 1–22. [Google Scholar] [CrossRef] [PubMed]
  135. Peñalver, R.; Lorenzo, J.M.; Ros, G.; Amarowicz, R.; Pateiro, M.; Nieto, G. Seaweeds as a Functional Ingredient for a Healthy Diet. Mar. Drugs 2020, 18, 301. [Google Scholar] [CrossRef]
  136. Liu, F.; Pang, S.; Gao, S.; Shan, T. Intraspecific genetic analysis, gamete release performance, and growth of Sargassum muticum (Fucales, Phaeophyta) from China. Chinese J. Oceanol. Limnol. 2013, 31, 1268–1275. [Google Scholar] [CrossRef]
  137. Yang, E.-J.; Ham, Y.M.; Lee, W.J.; Lee, N.H.; Hyun, C.-G. Anti-inflammatory effects of apo-9′-fucoxanthinone from the brown alga, Sargassum muticum. DARU J. Pharm. Sci. 2013, 21, 62. [Google Scholar] [CrossRef] [Green Version]
  138. Lodeiro, P.; Cordero, B.; Grille, Z.; Herrero, R.; Sastre de Vicente, M.E. Physicochemical studies of Cadmium(II) biosorption by the invasive alga in Europe, Sargassum muticum. Biotechnol. Bioeng. 2004, 88, 237–247. [Google Scholar] [CrossRef] [Green Version]
  139. Milledge, J.J.; Nielsen, B.V.; Bailey, D. High-value products from macroalgae: The potential uses of the invasive brown seaweed, Sargassum muticum. Rev. Environ. Sci. Biotechnol. 2016, 15. [Google Scholar] [CrossRef]
  140. Silva, L.D.; Bahcevandziev, K.; Pereira, L. Production of bio-fertilizer from Ascophyllum nodosum and Sargassum muticum (Phaeophyceae). J. Oceanol. Limnol. 2019, 37, 918–927. [Google Scholar] [CrossRef]
  141. Zhao, F.; Liu, F.; Liu, J.; Ang, P.O.; Duan, D. Genetic structure analysis of natural Sargassum muticum (Fucales, Phaeophyta) populations using RAPD and ISSR markers. J. Appl. Phycol. 2008, 20, 191–198. [Google Scholar] [CrossRef]
  142. Hay, C.H. The dispersal of sporophytes of Undaria pinnatifida by coastal shipping in New Zealand, and implications for further dispersal of Undaria in France. Br. Phycol. J. 1990, 25, 301–313. [Google Scholar] [CrossRef] [Green Version]
  143. Aguilar-Rosas, R.; Aguilar-Rosas, L.E.; Ávila-Serrano, G.; Marcos-Ramírez, R. First record of Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyta) on the Pacific coast of Mexico. Bot. Mar. 2004, 47. [Google Scholar] [CrossRef]
  144. Boudouresque, C.F.; Verlaque, M. Biological pollution in the Mediterranean Sea: Invasive versus introduced macrophytes. Mar. Pollut. Bull. 2002, 44, 32–38. [Google Scholar] [CrossRef]
  145. Floc’h, J.Y.; Pajot, R.; Wallentinus, I. The Japanese brown alga Undaria pinnatifida on the coast of France and its possible establishment in European waters. ICES J. Mar. Sci. 1991, 47, 379–390. [Google Scholar] [CrossRef]
  146. Silva, P.C.; Woodfield, R.A.; Cohen, A.N.; Harris, L.H.; Goddard, J.H.R. First Report of the Asian kelp Undaria pinnatifida in the Northeastern Pacific Ocean. Biol. Invasions 2002, 333–338. [Google Scholar] [CrossRef]
  147. Thornber, C.; Kinlan, B.; Graham, M.; Stachowicz, J. Population ecology of the invasive kelp Undaria pinnatifida in California: Environmental and biological controls on demography. Mar. Ecol. Prog. Ser. 2004, 268, 69–80. [Google Scholar] [CrossRef]
  148. Zabin, C.; Ashton, G.; Brown, C.; Ruiz, G. Northern range expansion of the Asian kelp Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyceae) in western North America. Aquat. Invasions 2009, 4, 429–434. [Google Scholar] [CrossRef]
  149. Curiel, D.; Bellemo, G.; Marzocchi, M.; Scattolin, M.; Parisi, G. Distribution of introduced Japanese macroalgae Undaria pinnatifida, Sargassum muticum (Phaeophyta) and Antithamnion Pectinatum (Rhodophyta) in the Lagoon of Venice. Hydrobiologia 1998, 385, 17–22. [Google Scholar] [CrossRef]
  150. Smith, J.; Summers, G.; Wong, R. Nutrient and heavy metal content of edible seaweeds in New Zealand. New Zeal. J. Crop Hortic. Sci. 2010, 38, 19–28. [Google Scholar] [CrossRef]
  151. Alga Desidratada Wakame—Poorto Muiños. Available online: https://www.elcorteingles.pt/supermercado/0105218175200239-porto-muinos-alga-desidratada-wakame-embalagem-50-g/ (accessed on 15 September 2020).
  152. Algas, L. Das Mexilhão ao Natural em Cama de Wakame—Porto Muiños. Available online: https://www.lojadasalgas.pt/index.php?route=product/product&product_id=145&search=wakame (accessed on 15 September 2020).
  153. Kolb, N.; Vallorani, L.; Milanović, N.; Stocchi, V. Evaluation of Marine Algae Wakame (Undaria pinnatifida) and Kombu (Laminaria digitata japonica) as Food Supplements. Food Technol. Biotechnol. 2004, 42, 57–61. [Google Scholar]
  154. Taira, H. Standard Tables of Food Composition in Japan, Fifth revised edition. J. Integr. Study Diet. Habits 2001, 48, 549–553. [Google Scholar]
  155. Taboada, M.C.; Millán, R.; Miguez, M.I. Nutritional value of the marine algae wakame (Undaria pinnatifida) and nori (Porphyra purpurea) as food supplements. J. Appl. Phycol. 2013, 25, 1271–1276. [Google Scholar] [CrossRef]
  156. González, A.; Paz, S.; Rubio, C.; Gutiérrez, Á.J.; Hardisson, A. Human Exposure to Iodine from the Consumption of Edible Seaweeds. Biol. Trace Elem. Res. 2020, 197, 361–366. [Google Scholar] [CrossRef] [PubMed]
  157. Ahn, J.; Ha, T.Y.; Ahn, J.; Jung, C.H.; Seo, D.H.; Kim, J.M.; Kim, Y.S.; Jang, Y. Undaria pinnatifida extract feeding increases exercise endurance and skeletal muscle mass by promoting oxidative muscle remodeling in mice. Faseb J. 2020, 34, 8068–8081. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  158. Patra, J.K.; Lee, S.; Park, J.A.E.G.Y.U.; Baek, K. Antioxidant and antibacterial properties of essential oil extracted from an edible seaweed Undaria pinnatifida. J. Food Biochem. 2017, 41, e12278. [Google Scholar] [CrossRef]
  159. Yoshinaga, K.; Maruya, R.; Koikeda, T.; Nakano, T. Effects of Undaria pinnatifida (wakame) on the human intestinal environment. Funct. Foods Heal. Dis. 2018, 8, 488–504. [Google Scholar] [CrossRef]
  160. Florencia, M.; Lorena, S.; Yamila, A.; Alejandra, M.; Fernando, D.; Alejandra, V.; Anahí, C. Amelioration of tomato plants cultivated in organic-matter impoverished soil by supplementation with Undaria pinnatifida. Algal Res. 2020, 46, 101785. [Google Scholar] [CrossRef]
  161. Verlaque, M.; Durand, C.; Huisman, J.M.; Parco, Y. Le On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). Eur. J. Phycol. 2010, 38, 325–339. [Google Scholar] [CrossRef] [Green Version]
  162. Klein, J.; Verlaque, M. The Caulerpa racemosa invasion: A critical review. Mar. Pollut. Bull. 2008, 56, 205–225. [Google Scholar] [CrossRef]
  163. Moderna, M.; Matricardi, G.; Vacchi, M.; Guidetti, P. Spreading of Caulerpa racemosa (Forsskl) J. Agardh (Bryopsidaceae, Chlorophyta) along the coasts of the Ligurian Sea. Cryptogam. Algol. 2000, 21, 301–304. [Google Scholar] [CrossRef]
  164. Nuber, N.; Gornik, O.; Lauc, G.; Bauer, N.; Žuljević, A.; Papeš, D.; Zoldoš, V. Genetic evidence for the identity of Caulerpa racemosa (Forsskål) J. Agardh (Caulerpales, Chlorophyta) in the Adriatic Sea. Eur. J. Phycol. 2007, 42, 113–120. [Google Scholar] [CrossRef]
  165. Martín, C.P.; Fernandez, J.C.C.; Crespo, M.B.; Poveda, M.S. Caulerpa racemosa (Forssk.) J. Agardh (Caulerpaceae, Chlorophyceae), nueva para la flora de Alicante. An. Jard. Bot. Madr. 2003, 60, 448–449. [Google Scholar]
  166. De Gaillande, C.; Payri, C.; Remoissenet, G.; Zubia, M. Caulerpa consumption, nutritional value and farming in the Indo-Pacific region. J. Appl. Phycol. 2017, 29, 2249–2266. [Google Scholar] [CrossRef]
  167. Freile-pelegrin, Y.; Robledo, D.; Pelegrín, Y.F. Chemical and Mineral Composition of Six Potentially Edible Seaweed Species of Yucatán Chemical and Mineral Composition of Six Potentially Edible Seameed Species of Yucatán. Bot. Mar. 1997, 40, 301–306. [Google Scholar] [CrossRef]
  168. Robledo, D.; Freile-pelegrin, Y. Seasonal variation in photosynthesis and biochemical composition of Caulerpa Seasonal variation in photosynthesis and biochemical composition of Caulerpa spp. (Bryopsidales, Chlorophyta) from the Gulf of Mexico. Phycologia 2005, 8884. [Google Scholar] [CrossRef]
  169. Nagappan, T.; Vairappan, C.S. Nutritional and bioactive properties of three edible species of green algae, genus Caulerpa (Caulerpaceae). J. Appl. Phycol. 2014, 26, 1019–1027. [Google Scholar] [CrossRef]
  170. Kumar, M.; Gupta, V.; Kumari, P.; Reddy, C.R.K.; Jha, B. Assessment of nutrient composition and antioxidant potential of Caulerpaceae seaweeds. J. Food Compos. Anal. 2001, 24, 270–278. [Google Scholar] [CrossRef]
  171. Ghosh, P.; Adhikari, U.; Ghosal, P.K.; Pujol, C.A.; Carlucci, M.J.; Damonte, E.B.; Ray, B. In vitro anti-herpetic activity of sulfated polysaccharide fractions from Caulerpa racemosa. Phytochemistry 2004, 65, 3151–3157. [Google Scholar] [CrossRef]
  172. Ribeiro, N.A.; Abreu, T.M.; Chaves, H.V.; Bezerra, M.M.; Monteiro, H.S.A.; Jorge, R.J.B.; Benevides, N.M.B. Sulfated polysaccharides isolated from the green seaweed Caulerpa racemosa plays antinociceptive and anti-inflammatory activities in a way dependent on HO-1 pathway activation. Inflamm. Res. 2014, 63, 569–580. [Google Scholar]
  173. Kathiraven, T.; Sundaramanickam, A.; Shanmugam, N.; Balasubramanian, T. Green synthesis of silver nanoparticles using marine algae Caulerpa racemosa and their antibacterial activity against some human pathogens. Appl. Nanosci. 2015, 5. [Google Scholar] [CrossRef] [Green Version]
  174. Matanjun, P.; Mohamed, S.; Mustapha, N.M.; Muhammad, K.; Ming, C.H.A. Antioxidant activities and phenolics content of eight species of seaweeds from north Borneo. J. Appl. Phycol. 2008, 20, 367–373. [Google Scholar]
  175. Lucas, A.H.S. The marine algae of Lord Howe Island. Proc. Linn. Soc. N. S. W. 1935, 60, 194–232. [Google Scholar]
  176. Capiomont, A.; Breugnot, E.; Haan, M.D.; Meinesz, A. Phenology of a deep-water population of Caulerpa racemosa var. cylindracea in the northwestern Mediterranean Sea. Bot. Mar. 2005, 48, 80–83. [Google Scholar]
  177. Thibaut, T.; Meinesz, A.; Coquillard, P. Biomass seasonality of Caulerpa taxifolia in the Mediterranean Sea. Aquat. Bot. 2004, 80, 291–297. [Google Scholar] [CrossRef]
  178. Boudouresque, C.F. Caulerpa taxifolia: The great escape. World Conserv. 1998, 97, 17–18. [Google Scholar]
  179. Amade, P.; Lemee, R. Chemical defence of the Mediterranean alga Caulerpa taxifolia: Variations in caulerpenyne production. Aquat. Toxicol. 1998, 43, 287–300. [Google Scholar] [CrossRef]
  180. Sureda, A.; Box, A.; Ensenat, M.; Alou, E.; Tauler, P.; Deudero, S.; Pons, A. Enzymatic antioxidant response of a labrid fish (Coris julis) liver to environmental caulerpenyne. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2006, 144, 191–196. [Google Scholar] [CrossRef]
  181. Bellansantini, D.; Arnaud, P.M.; Bellan, G.; Verlaque, M. The influence of the introduced tropical alga Caulerpa taxifolia, on the biodiversity of the Mediterranean marine biota. J. Mar. Biol. Assoc. UK 1996, 76. [Google Scholar] [CrossRef]
  182. Fischel, J.L.; Lemee, R.; Formento, P.; Caldani, C.; Moll, J.L.; Pesando, D.; Meinesz, A.; Grelier, P.; Pietra, P.; Guerriero, A. Cell-growth-inhibitory effects of caulerpenyne, a sesquiterpenoid from the marine alga Caulerpa taxifolia. Anticancer Res. 1995, 15, 2155–2160. [Google Scholar]
  183. Silva, P. The dichotomous species of Codium in Britain. J. Mar. Biol. Assoc. United Kingdom 1955, 34, 565–577. [Google Scholar] [CrossRef] [Green Version]
  184. Trowbridge, C.D. Ecology of the green macroalga Codium fragile (Suringar) Hariot: Invasive and noninvasive subspecies. Oceanogr. Mar. Biol. Annu. Rev. 1998, 36. [Google Scholar]
  185. Nyberg, C.D.; Wallentinus, I. Can species traits be used to predict marine macroalgal introductions? Biol. Invasions 2005, 7, 265–279. [Google Scholar] [CrossRef] [Green Version]
  186. Chapman, A.S.; Stévant, P.; Larssen, W.E. Food or fad? Challenges and opportunities for including seaweeds in a Nordic diet. Bot. Mar. 2015, 58, 423–433. [Google Scholar] [CrossRef]
  187. Schmidt, A.L.; Scheibling, R.E. Effects of native and invasive macroalgal canopies on composition and abundance of mobile benthic macrofauna and turf-forming algae. J. Exp. Mar. Bio. Ecol. 2007, 341, 110–130. [Google Scholar] [CrossRef]
  188. Scheibling, R.E. Species Invasions and Community Change Threaten the Sea Urchin Fishery in Nova Scotia. L’atelier sur la Coordination de la Researche sur L’oursin Vert au Canada Atlantique. Available online: http://crdpm.umcs.ca/OURSIN/PDF/SCHEIB.PDF (accessed on 16 September 2020).
  189. Watanabe, S.; Metaxas, A.; Scheibling, R.E. Dispersal potential of the invasive green alga Codium fragile ssp. fragile. J. Exp. Mar. Bio. Ecol. 2009, 381, 114–125. [Google Scholar] [CrossRef]
  190. Xu, X.Q.; Tran, V.H.; Kraft, G.; Beardall, J. Fatty acids of six Codium species from southeast Australia. Phytochemistry 1998, 48, 1335–1339. [Google Scholar] [CrossRef]
  191. Herbreteau, F.; Coiffard, L.J.M.; Derrien, A.; De Roeck-Holtzhauer, Y. The fatty acid composition of five species of macroalgae. Bot. Mar. 1997, 40, 2155–2160. [Google Scholar] [CrossRef]
  192. Wang, J.; Jin, W.; Hou, Y.; Niu, X.; Zhang, H.; Zhang, Q. Chemical composition and moisture-absorption/retention ability of polysaccharides extracted from five algae. Int. J. Biol. Macromol. 2013, 57. [Google Scholar] [CrossRef]
  193. Rojo, I.; Olabarria, C.; Santamaria, M.; Provan, J.; Gallardo, T.; Viejo, R.M. Coexistence of congeneric native and invasive species: The case of the green algae Codium spp. in northwestern spain. Mar. Environ. Res. 2014, 101, 135–144. [Google Scholar] [CrossRef]
  194. Hafting, J.T.; Craigie, J.S.; Stengel, D.B.; Loureiro, R.R.; Buschmann, A.H.; Yarish, C.; Edwards, M.D.; Critchley, A.T. Prospects and challenges for industrial production of seaweed bioactives. J. Phycol. 2015, 51, 821–837. [Google Scholar] [CrossRef]
  195. Wang, Y.; Xing, M.; Cao, Q.; Ji, A.; Liang, H.; Song, S. Biological activities of fucoidan and the factors mediating its therapeutic effects: A review of recent studies. Mar. Drugs 2019, 17, 183. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  196. Pereira, L. Therapeutic and Nutritional Uses of Algae; Pereira, L., Ed.; CRC Press: Boca Raton, FL, USA, 2018; ISBN 9781315152844. [Google Scholar]
  197. Yang, L.; Lu, Q.; Brodie, J. A review of the bladed Bangiales (Rhodophyta) in China: History, culture and taxonomy. Eur. J. Phycol. 2017, 52, 251–263. [Google Scholar] [CrossRef]
  198. Gacesa, R.; Lawrence, K.P.; Georgakopoulos, N.D.; Yabe, K.; Dunlap, W.C.; Barlow, D.J.; Wells, G.; Young, A.R.; Long, P.F. The mycosporine-like amino acids porphyra-334 and shinorine are antioxidants and direct antagonists of Keap1-Nrf2 binding. Biochimie 2018, 154, 35–44. [Google Scholar] [CrossRef] [PubMed]
  199. Zhang, Z.; Zhang, Q.; Wang, J.; Song, H.; Zhang, H.; Niu, X. Regioselective syntheses of sulfated porphyrans from Porphyra haitanensis and their antioxidant and anticoagulant activities in vitro. Carbohydr. Polym. 2010, 79, 1124–1129. [Google Scholar] [CrossRef]
  200. Cian, R.E.; Fajardo, M.A.; Alaiz, M.; Vioque, J.; González, R.J.; Drago, S.R. Chemical composition, nutritional and antioxidant properties of the red edible seaweed Porphyra columbina. Int. J. Food Sci. Nutr. 2014, 65, 299–305. [Google Scholar] [CrossRef] [Green Version]
  201. Qu, W.; Ma, H.; Li, W.; Pan, Z.; Owusu, J.; Venkitasamy, C. Performance of coupled enzymatic hydrolysis and membrane separation bioreactor for antihypertensive peptides production from Porphyra yezoensis protein. Process Biochem. 2015, 50, 245–252. [Google Scholar] [CrossRef]
  202. Qu, W.; Ma, H.; Pan, Z.; Luo, L.; Wang, Z.; He, R. Preparation and antihypertensive activity of peptides from Porphyra yezoensis. Food Chem. 2010, 123, 14–20. [Google Scholar] [CrossRef]
  203. Sakai, S.; Komura, Y.; Nishimura, Y.; Sugawara, T.; Hirata, T. Inhibition of mast cell degranulation by phycoerythrin and its pigment moiety phycoerythrobilin, prepared from Porphyra yezoensis. Food Sci. Technol. Res. 2011, 17, 171–177. [Google Scholar] [CrossRef] [Green Version]
  204. Kwon, M.-J.; Nam, T.-J. Porphyran induces apoptosis related signal pathway in AGS gastric cancer cell lines. Life Sci. 2006, 79, 1956–1962. [Google Scholar] [CrossRef]
  205. Yu, X.; Zhou, C.; Yang, H.; Huang, X.; Ma, H.; Qin, X.; Hu, J. Effect of ultrasonic treatment on the degradation and inhibition cancer cell lines of polysaccharides from Porphyra yezoensis. Carbohydr. Polym. 2015, 117, 650–656. [Google Scholar] [CrossRef]
  206. Indumathi, P.; Mehta, A. A novel anticoagulant peptide from the Nori hydrolysate. J. Funct. Foods 2016, 20, 606–617. [Google Scholar] [CrossRef]
  207. Liu, Q.; Xu, S.; Li, L.; Pan, T.; Shi, C.; Liu, H.; Cao, M.; Su, W.; Liu, G. In vitro and in vivo immunomodulatory activity of sulfated polysaccharide from Porphyra haitanensis. Carbohydr. Polym. 2017, 165, 189–196. [Google Scholar] [CrossRef] [PubMed]
  208. Nishiguchi, T.; Cho, K.; Isaka, S.; Ueno, M.; Jin, J.-O.; Yamaguchi, K.; Kim, D.; Oda, T. Protective effect of porphyran isolated from discolored nori (Porphyra yezoensis) on lipopolysaccharide-induced endotoxin shock in mice. Int. J. Biol. Macromol. 2016, 93, 1273–1278. [Google Scholar] [CrossRef] [PubMed]
  209. Jiang, Z.; Hama, Y.; Yamaguchi, K.; Oda, T. Inhibitory effect of sulphated polysaccharide porphyran on nitric oxide production in lipopolysaccharide-stimulated RAW264.7 macrophages. J. Biochem. 2012, 151, 65–74. [Google Scholar] [CrossRef] [Green Version]
  210. Cian, R.E.; López-Posadas, R.; Drago, S.R.; de Medina, F.S.; Martínez-Augustin, O. Immunomodulatory Properties of the Protein Fraction from Phorphyra columbina. J. Agric. Food Chem. 2012, 60, 8146–8154. [Google Scholar] [CrossRef] [PubMed]
  211. Wang, X.; He, L.; Ma, Y.; Huan, L.; Wang, Y.; Xia, B. Economically important red algae resources along the Chinese coast: History, status, and prospects for their utilization. Algal Res. 2020, 46, 101817. [Google Scholar] [CrossRef]
  212. Yakuhin, B. Evaluation of combined deactivators-supplemented agar medium (CDSAM) for recovery of dermatophytes from patients with tinea pedis. 2007, 2006–2008. [Google Scholar] [CrossRef] [Green Version]
  213. Yew, W.W.; Tong, S.C.W.; Lui, K.S.; Leung, S.K.F.; Chau, C.H.; Wang, E.P. Comparison of MB / BacT system and agar proportion method in drug susceptibility testing of Mycobacterium tuberculosis. Diagn. Microbiol. Infect. Dis. 2001, 39, 229–232. [Google Scholar] [CrossRef]
  214. Thakur, S.S.; Rupenthal, I.D. Validation of hyaluronic acid-agar-based hydrogels as vitreous humor mimetics for in vitro drug and particle migration evaluations. Eur. J. Pharm. Biopharm. 2020, 148, 118–125. [Google Scholar] [CrossRef]
  215. Munier, M.; Moranc, M.; Dumay, J.; Jaouen, P.; Fleurence, J. One-step purification of R-phycoerythrin from the red edible seaweed Grateloupia turuturu. J. Chromatogr. B 2015, 992, 23–29. [Google Scholar] [CrossRef]
  216. Denis, C.; Massé, A.; Fleurence, J.; Jaouen, P. Concentration and pre-purification with ultrafiltration of a R-phycoerythrin solution extracted from macro-algae Grateloupia turuturu: Process definition and up-scaling. Sep. Purif. Technol. 2009, 69, 37–42. [Google Scholar] [CrossRef]
  217. Cardoso, I.; Cotas, J.; Rodrigues, A.; Ferreira, D.; Osório, N.; Pereira, L. Extraction and analysis of compounds with antibacterial potential from the red alga Grateloupia turuturu. J. Mar. Sci. Eng. 2019, 7, 220. [Google Scholar] [CrossRef] [Green Version]
  218. Alves, C.; Pinteus, S.; Rodrigues, A.; Horta, A.; Pedrosa, R. Algae from Portuguese Coast Presented High Cytotoxicity and Antiproliferative Effects on an in vitro Model of Human Colorectal Cancer. Pharmacognosy Res. 2018, 10, 24–30. [Google Scholar] [CrossRef] [PubMed]
  219. Vitale, F.; Genovese, G.; Bruno, F.; Castelli, G.; Piazza, M.; Migliazzo, A.; Minicante, S.A.; Manghisi, A.; Morabito, M. Effectiveness of red alga Asparagopsis taxiformis extracts against Leishmania infantum. Open Life Sci. 2015, 10, 490–496. [Google Scholar] [CrossRef]
  220. Genovese, G.; Leitner, S.; Minicante, S.A.; Lass-Flörl, C. The Mediterranean red alga Asparagopsis taxiformis has antifungal activity against Aspergillus species. Mycoses 2013, 56, 516–519. [Google Scholar] [CrossRef] [PubMed]
  221. Arunkumar, K.; Raja, R.; Kumar, V.B.S.; Joseph, A.; Shilpa, T.; Carvalho, I.S. Antioxidant and cytotoxic activities of sulfated polysaccharides from five different edible seaweeds. J. Food Meas. Charact. 2020. [Google Scholar] [CrossRef]
  222. Alburquerque, N.; Faize, L.; Faize, M.; Nortes, M.D.; Bernardeau, J.; Fernandez, J.M.R.; Burgos, L. Towards the valorization of the invasive seaweeds Caulerpa cylindracea and Asparagopsis taxiformis in the Mediterranean Sea: Applications for in vitro plant regeneration and crop protection. J. Appl. Phycol. 2019, 31, 1403–1413. [Google Scholar] [CrossRef]
  223. Rostami, Z.; Tabarsa, M.; You, S.G.; Rezaei, M. Structural characterization and RAW264.7 murine macrophage stimulating activity of a fucogalactoglucan from Colpomenia peregrina. J. Food Sci. Technol. 2018, 55, 4650–4660. [Google Scholar] [CrossRef]
  224. Lee, J.A.; Cho, Y.-R.; Hong, S.S.; Ahn, E.-K. Anti-Obesity Activity of Saringosterol Isolated from Sargassum muticum (Yendo) Fensholt Extract in 3T3-L1 Cells. Phyther. Res. 2017, 31, 1694–1701. [Google Scholar] [CrossRef]
  225. Yu, Y.; Wang, L.; Fu, X.; Wang, L.; Fu, X.; Yang, M.; Han, Z.; Mou, H.; Jeon, Y.-J. Anti-oxidant and anti-inflammatory activities of ultrasonic-assistant extracted polyphenol-rich compounds from Sargassum muticum. J. Oceanol. Limnol. 2019, 37, 836–847. [Google Scholar] [CrossRef]
  226. Félix, R.; Félix, C.; Januário, A.P.; Carmona, A.M.; Baptista, T.; Gonçalves, R.A.; Sendão, J.; Novais, S.C.; Lemos, M.F.L. Tailoring shrimp aquafeed to tackle Acute Hepatopancreatic Necrosis Disease by inclusion of industry-friendly seaweed extracts. Aquaculture 2020, 529, 735661. [Google Scholar] [CrossRef]
  227. Mohammed, A.; Rivers, A.; Stuckey, D.C.; Ward, K. Alginate extraction from Sargassum seaweed in the Caribbean region: Optimization using response surface methodology. Carbohydr. Polym. 2020, 245, 116419. [Google Scholar] [CrossRef] [PubMed]
  228. González-López, N.; Moure, A.; Domínguez, H. Hydrothermal fractionation of Sargassum muticum biomass. J. Appl. Phycol. 2012, 24, 1569–1578. [Google Scholar] [CrossRef]
  229. Pereira, L.; Cotas, J. Introductory Chapter: Alginates - A General Overview. In Alginates - Recent Uses of This Natural Polymer; IntechOpen: London, UK, 2020. [Google Scholar]
  230. Phull, A.R.; Kim, S.J. Undaria pinnatifida a Rich Marine Reservoir of Nutritional and Pharmacological Potential: Insights into Growth Signaling and Apoptosis Mechanisms in Cancer. Nutr. Cancer 2019, 70, 956–970. [Google Scholar]
  231. Ayyad, S.E.; Badria, F.A. Caulerpine: An antitumorindele alkaloid from Caulerpa racemosa. Alex. J. Pharm. Sci. 1994, 8, 217–219. [Google Scholar]
  232. Rocha, F.D.; Soares, A.R.; Houghton, P.J.; Crespo, R.; Auxiliadora, M.; Kaplan, C.; Teixeira, V.L. Potential cytotoxic activity of some brazilian seaweeds on human Melanoma Cells. Phytother. Res. 2007, 21, 170–175. [Google Scholar] [CrossRef]
  233. De Souza, É.T.; De Lira, D.P.; De Queiroz, A.C.; José, D.; De Aquino, A.B.; Lorenzo, V.P.; De Miranda, G.E.C.; De Araújo-júnior, J.X.; Célia, M.; Chaves, D.O. The antinociceptive and anti-inflammatory activities of caulerpin, a bisindole alkaloid isolated from seaweeds of the genus Caulerpa. Mar. Drugs 2009, 7, 689–704. [Google Scholar] [CrossRef] [Green Version]
  234. Del Coco, L.; Felline, S.; Girelli, C.R.; Angil, F.; Magliozzi, L.; Almada, F.; Aniello, B.D.; Mollo, E.; Terlizzi, A.; Fanizzi, F.P. 1 H NMR Spectroscopy and MVA to evaluate the effects of caulerpin-based diet on Diplodus sargus lipid profiles. Mar. Drugs 2018, 16, 390. [Google Scholar] [CrossRef] [Green Version]
  235. Wang, L.; Young, J.; Geon, J.; Jayawardena, T.U.; Kim, Y.; Young, J.; Fu, X.; Jeon, Y. Protective effects of sulfated polysaccharides isolated from the enzymatic digest of Codium fragile against hydrogen peroxide-induced oxidative stress in in vitro and in vivo models. Algal Res. 2020, 48, 101891. [Google Scholar] [CrossRef]
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Figure 1. Seaweed (Pyropia sp.) pie with carrot and coconut.
Figure 1. Seaweed (Pyropia sp.) pie with carrot and coconut.
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Figure 2. Agarophyton vermiculophyllum collected in an aquaculture fish tank at Ria de Aveiro (Portugal).
Figure 2. Agarophyton vermiculophyllum collected in an aquaculture fish tank at Ria de Aveiro (Portugal).
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Figure 3. Underwater photography of Grateloupia turuturu in Buarcos Bay (Figueira da Foz, Portugal).
Figure 3. Underwater photography of Grateloupia turuturu in Buarcos Bay (Figueira da Foz, Portugal).
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Figure 4. Underwater photo of Asparagopsis armata in São Martinho do Porto (Portugal).
Figure 4. Underwater photo of Asparagopsis armata in São Martinho do Porto (Portugal).
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Figure 5. Underwater photo of Asparagopsis taxiformis in Terceira island (Azores archipelago -Portugal).
Figure 5. Underwater photo of Asparagopsis taxiformis in Terceira island (Azores archipelago -Portugal).
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Figure 6. Colpomenia peregrina in São Martinho do Porto (Portugal).
Figure 6. Colpomenia peregrina in São Martinho do Porto (Portugal).
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Figure 7. Sargassum muticum in Buarcos Bay (Figueira da Foz, Portugal).
Figure 7. Sargassum muticum in Buarcos Bay (Figueira da Foz, Portugal).
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Figure 8. Undaria pinnatifida in Buarcos Bay (Portugal).
Figure 8. Undaria pinnatifida in Buarcos Bay (Portugal).
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Figure 9. Underwater photography of C. racemosa in the Spanish islands.
Figure 9. Underwater photography of C. racemosa in the Spanish islands.
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Table
Table 1. Exotic seaweed species recorded in the Iberian Peninsula. R–Rhodophyta; O–Ochrophyta; C–Chlorophyta.
Table 1. Exotic seaweed species recorded in the Iberian Peninsula. R–Rhodophyta; O–Ochrophyta; C–Chlorophyta.
PhylumSpeciesSpainPortugalNative HabitatReferences
RAcrothamnion preissii (Sonder) E.M. Wollaston 1968x Australia[19]
RAgardhiella subulata (C. Agardh) Kraft and M.J. Wynne 1979x Canada[20]
RAgarophyton vermiculophyllum (Ohmi) Gurgel, J.N. Norris (formerly Gracilariopsis vermiculophylla Ohmi et Fredericq 2018)xxJapan[20,21]
RAsparagopsis armata Harvey 1855xxAustralia[20,22,23]
RAsparagopsis taxiformis (Delile) Trevisan 1845xxAustralia[22,23,24]
RBonnemaisonia hamifera Hariot 1891xxJapan[21]
RBotryocladia wrightii (Harvey) W.E. Schmidt, D.L. Ballantine and Fredericq 2017 (formerly Chrysymenia wrightii (Harvey) Yamada 1932)xxJapan[20,21]
RCallithamniella flexilis Baardseth 1941x Stoltenhoff Island (South Atlantic)[20]
RContarinia squamariae (Meneghini) Denizot 1968 (formerly Wormskioldia squamariae Meneghini) x-[21]
RDasya sessilis Yamada 1928xxJapan[21]
RDasysiphonia japonica (Yendo) H.–S. Kim 2012x Japan[21]
RFalkenbergia rufolanosa (Harvey) F. Schmitz 1897xxAustralia[20,25]
RGracilariopsis chorda (Holmes) Ohmi 1958x Japan[26]
RGrateloupia filicina (J.V. Lamouroux) C. Agardh 1822xxAustralia[21]
RGrateloupia subpectinata Holmes 1912xxJapan[20,21]
RGrateloupia turuturu Yamada 1941xxJapan[21]
RGulsonia nodulosa (Ercegovic) Feldmann and G. Feldmann 1967 xAdriatic[21]
RKapraunia schneideri (Stuercke and Freshwater) A.M. Savoie and G.W.Saunders 2019 (formerly Polysiphonia schneideri B. Stuercke and D.W. Freshwater)x North America (North Carolina)[21]
RLomentaria hakodatensis Yendo 1920xxJapan[20]
RLophocladia lallemandii (Montagne) F. Schmitz 1893.x Egypt (Suez channel)[21]
RMelanothamnus harveyi (Bailey) Díaz-Tapia and Maggs 2017 (formerly Neosiphonia harveyi (Bailey) M.-S. Kim, H.-G. Choi, Guiry and G.W. Saunders 2001)xxNorth America (Connecticut)[20,21]
RPachymeniopsis lanceolata (K. Okamura) Y. Yamada ex S. Kawabata 1954x Japan[27]
RPolysiphonia morrowii Harvey 1857x Japan or Korea[20]
RPyropia suborbiculata (Kjellman) J.E. Sutherland, H.G. Choi, M.S. Hwang and W.A. Nelson 2011xxJapan[20,21]
RScageliopsis patens E.M. Wollaston 1981xxAustralia[20,21]
RSymphyocladia marchantioides (Harvey) Falkenberg 1897 xNew Zealand[20,21]
RWomersleyella setacea (Hollenberg) R.E. Norris 1992x Hawaii[21]
OColpomenia peregrina Sauvageau 1927xxPacific coast of North America[23]
ODictyota cyanoloma Tronholm, De Clerck, A. Gómez-Garreta and Rull Lluch 2010x Australia[19]
OSargassum muticum (Yendo) Fensholt 1955xxJapan[21]
OScytosiphon dotyi M.J. Wynne 1969 xNorth America (California)[21]
OStypopodium schimperi (Kützing) Verlaque and Boudouresque 1991x Egypt (Sinai Peninsula)[21]
OUndaria pinnatifida (Harvey) Suringar 1873xxJapan[21]
OZosterocarpus oedogonium (Meneghini) Bornet 1890 xMediterranean[19]
CCaulerpa racemosa (Forsskål) J. Agardh 1873x Australia[21]
CCaulerpa taxifolia (M. Vahl) C. Agardh 1817x India[19]
CCaulerpa cylindracea Sonder 1845x Australia[19]
CCodium arabicum Kützing 1856 xEgypt[19]
CCodium fragile subsp. fragile (Suringar) Hariot 1889xxJapan[21]
CUlva australis Areschoug 1854x Japan[21]
Table
Table 2. Asparagopsis taxiformis nutritional characterization from biomass collected in different sampling sites. ND–Non-determined.
Table 2. Asparagopsis taxiformis nutritional characterization from biomass collected in different sampling sites. ND–Non-determined.
Harvesting SiteLipidsProteinsCarbohydratesAshMoistureReference
Madeira Archipelago (% DW)6.6223.7632.47N.D.4.50[73]
Hawaii (%)46.113.23690.03[74]
Egypt (% DW)0.40.517.9NDND[75]
Table
Table 3. Micronutrient and trace element composition of the red seaweeds G. turuturu, A. armata, and A. taxiformis according to Rodrigues et al. (2015), Roque et al. (2019), and Selmi et al. (2020) [70,76,77], and the nutrient value reference (NVR) for each element according to the European Food Safety Authority (ND–Non-determined; (a) % DW; (b) mg/day; (c) mg/kg bw/week).
Table 3. Micronutrient and trace element composition of the red seaweeds G. turuturu, A. armata, and A. taxiformis according to Rodrigues et al. (2015), Roque et al. (2019), and Selmi et al. (2020) [70,76,77], and the nutrient value reference (NVR) for each element according to the European Food Safety Authority (ND–Non-determined; (a) % DW; (b) mg/day; (c) mg/kg bw/week).
ElementElement Concentration (mg/g DW)NVR (mg)
G. turuturuA. armataA. taxiformis
MicronutrientsK20ND0.137842000
Mg21.38 (a)ND375
Ca2.654.47 (a)ND800
Na96.089.36 (a)0.200600
P2.810.27 (a)0.03593700
Trace elementsCu0.01ND0.481
Zn0.07NDND10
Fe0.051.1880.218914
Mn0.020.06230.003052
B0.020.0663ND10 (b)
Al0.010.0133ND1 (c)
AsNDND4 × 10−40.015 (c)
CdNDND2 × 10−50.007 (c)
HgNDND2 × 10−50.004 (c)
PbNDND5.1 × 10−40.005 (c)
Table
Table 4. Micronutrients and trace elements in the composition of Colpomenia peregrina in South West England (U.K.) according to Beacham et al. (2019) [118] and the nutrient value reference (NVR) for each element according to the European Food Safety Authority (a) mg/day; (b) mg/kg bw/week).
Table 4. Micronutrients and trace elements in the composition of Colpomenia peregrina in South West England (U.K.) according to Beacham et al. (2019) [118] and the nutrient value reference (NVR) for each element according to the European Food Safety Authority (a) mg/day; (b) mg/kg bw/week).
Biochemical profileElementConcentration (mg/g)NVR (mg)
MicronutrientsK46.932000
P0.67700
Ca55.64800
Trace ElementsCu0.021
Zn0.0510
Sn0.050.055
Mn0.232
Si252.2920–50 (a)
Al19.611 (b)
Fe9.3114
Table
Table 5. Sargassum muticum nutritional characterization from biomass collected in different sampling sites. ND–Non-determined.
Table 5. Sargassum muticum nutritional characterization from biomass collected in different sampling sites. ND–Non-determined.
Harvesting SiteLipidsProteinsCarbohydratesAshMoistureReference
U.K. (% DW)1.64.646926.4ND[118]
India (% FW)0.125.3139.2516.9087.91[132]
Spain (% DW)1.6–3.27–2227.9–44.513.2–30.5ND[133]
Portugal (% DW)1.4516.949.322.949.64[70]
Table
Table 6. Micronutrients and trace elements composition of Sargassum muticum harvested in the U.K. [118], India [132], and Spain [133] and the nutrient value reference (NVR) for each element, according to the European Food Safety Authority. ND–Non-dentermined; (a) mg/kg bw/week.
Table 6. Micronutrients and trace elements composition of Sargassum muticum harvested in the U.K. [118], India [132], and Spain [133] and the nutrient value reference (NVR) for each element, according to the European Food Safety Authority. ND–Non-dentermined; (a) mg/kg bw/week.
Biochemical ProfileElement (mg/g)CountryNVR (mg)
U.K.IndiaSpain
MicronutrientsK75.761326.252000
P1.340.4528ND700
Ca11.215.25647.15800
NaNDND13.75600
Trace ElementsFe0.080.5370.914
Sn0.06NDND0.055
Mn0.010.0250.032
Al0.28NDND1 (a)
CuND0.0030.01551
Zn0.010.1280.0267510
CrND0.005ND0.04
MoND0.001ND0.05
INDND0.00770.15
Ars NDND0.02160.015 (a)
Table
Table 7. Undaria pinnatifida nutritional macronutrient characterization from biomass collected in different sampling sites. ND–Not determined.
Table 7. Undaria pinnatifida nutritional macronutrient characterization from biomass collected in different sampling sites. ND–Not determined.
Harvesting SiteLipidsProteinsCarbohydratesFibersAshReference
Japan (Commercial sample % DW)3.1314.2145.08ND.37.58[153]
Japan (% DW)3.21535.32.730.8[154]
Spain (% DW)116.83714.928.3[155]
New Zealand (% DW)3.3019.6650.4ND26.58[150]
Table
Table 8. Undaria pinnatifida micronutrients and trace elements characterization comparatively to the native and invasive site according to the literature [153,155] and the nutrient value reference (NVR) for each element, according to the European Food Safety Authority. ND–Non-determined; (a) µg/kg bw/d.
Table 8. Undaria pinnatifida micronutrients and trace elements characterization comparatively to the native and invasive site according to the literature [153,155] and the nutrient value reference (NVR) for each element, according to the European Food Safety Authority. ND–Non-determined; (a) µg/kg bw/d.
Biochemical ProfileElement (mg/100g DW)CountryNVR (mg)
JapanSpain
MicronutrientsK569156792000
P4501070700
Ca950693.2800
Mg405630.2375
Na64943511600
Trace ElementsMn0.3320.692
Ni0.265ND2.8 (a)
Cu0.1850,191
Zn0.9443,8610
Cr0.072ND0.04
I269.60.15
Table
Table 9. Micronutrients and trace elements in the composition of Caulerpa racemosa in India, according to Kumar et al. (2001) [170], and the nutrient value reference (NVR) for each element, according to the European Food Safety Authority.
Table 9. Micronutrients and trace elements in the composition of Caulerpa racemosa in India, according to Kumar et al. (2001) [170], and the nutrient value reference (NVR) for each element, according to the European Food Safety Authority.
Biochemical ProfileElementConcentration (% DW)NVR (mg)
MicronutrientsK5.032000
Ca4.76800
Mg4.161375
Na10.64600
Trace ElementsFe29.7114
Mn4.912
Mo0.150.05
Cu0.621
Zn6.8210
Se0.130.055
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Pacheco, D.; Araújo, G.S.; Cotas, J.; Gaspar, R.; Neto, J.M.; Pereira, L. Invasive Seaweeds in the Iberian Peninsula: A Contribution for Food Supply. Mar. Drugs 2020, 18, 560. https://doi.org/10.3390/md18110560

AMA Style

Pacheco D, Araújo GS, Cotas J, Gaspar R, Neto JM, Pereira L. Invasive Seaweeds in the Iberian Peninsula: A Contribution for Food Supply. Marine Drugs. 2020; 18(11):560. https://doi.org/10.3390/md18110560

Chicago/Turabian Style

Pacheco, Diana, Glacio Souza Araújo, João Cotas, Rui Gaspar, João M. Neto, and Leonel Pereira. 2020. "Invasive Seaweeds in the Iberian Peninsula: A Contribution for Food Supply" Marine Drugs 18, no. 11: 560. https://doi.org/10.3390/md18110560

APA Style

Pacheco, D., Araújo, G. S., Cotas, J., Gaspar, R., Neto, J. M., & Pereira, L. (2020). Invasive Seaweeds in the Iberian Peninsula: A Contribution for Food Supply. Marine Drugs, 18(11), 560. https://doi.org/10.3390/md18110560

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