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.

Table 1. Exotic seaweed species recorded in the Iberian Peninsula. R–Rhodophyta; O–Ochrophyta; C–Chlorophyta.

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.

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].

Figure 1. Seaweed (Pyropia sp.) pie with carrot and coconut.

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].

Figure 2. Agarophyton vermiculophyllum collected in an aquaculture fish tank at Ria de Aveiro (Portugal).

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].

Figure 3. Underwater photography of Grateloupia turuturu in Buarcos Bay (Figueira da Foz, Portugal).

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.

Table 2. Asparagopsis taxiformis nutritional characterization from biomass collected in different sampling sites. ND–Non-determined.

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).

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.

Figure 4. Underwater photo of Asparagopsis armata in São Martinho do Porto (Portugal).

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].

Figure 5. Underwater photo of Asparagopsis taxiformis in Terceira island (Azores archipelago -Portugal).

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 × 10⁻⁴mg/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 × 10⁻⁵mg/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].

Figure 6. Colpomenia peregrina in São Martinho do Porto (Portugal).

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).

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).

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].