Seaweed Aquaculture Importance in Sustainable Economy in an Era of Climate Change

Abstract

Seaweeds have been used globally for different purposes. Recent developments in technology coupled with an increasing interest in the resource have created a need for seaweed aquaculture to meet the demand. This review tackles the question of whether seaweed aquaculture has the potential to support the blue economy as well as climate change adaptation. Seaweed aquaculture represents an economically viable sector that has the potential to support the blue economy. The sector succeeds in meeting sustainability requirements while supporting human health and wealth through qualities such as naturally acting as a bio-filter, reducing ocean acidification, carbon sequestration, provision of habitat, and coastal protection; seaweed aquaculture can be used as a tool in conservation and climate adaptation. However, seaweed aquaculture is still in its infancy in many areas of the world, especially in the West, and there is a need for improved legislation and guidelines. Furthermore, several environmental hazards, such as physical stress (abiotic and abiotic factors), genetic depletion, and the introduction of non-native species, can cause future problems, particularly if legislation restrictions are not fully revised to ensure the safety of seaweed aquaculture. The sector poses great opportunities and is a sustainable way forward that is necessary to meet increasing demand.

1. Introduction

Seaweed has been used by humans for centuries for different purposes such as nutrition, medicine, and fertilizer [1, 2, 3]. This group of marine plants, also referred to as macroalgae, is composed of three taxonomic groups: brown (Ochrophyta, Phaeophyceae), red (Rhodophyta), and green (Chlorophyta) seaweeds [4, 5]. They are distributed horizontally in different zones, which are supratidal (supralittoral), intertidal (littoral), and subtidal (sublittoral) regions of the seas and oceans [4]. Green, brown, and red seaweeds are generally distributed in the intertidal, tidal, or upper subtidal zone and subtidal regions, respectively [6].

The presence of seaweeds in all climate belts, great biodiversity, their compositional abundance of vitamins and macro- and micronutrients, and the fact that most seaweeds are edible suggest that seaweeds have played an important role as human food during human evolution. Seaweeds have served as a cheap and easily accessible crop in the daily fare for coastal populations, especially in Southeast Asia, where seaweeds have for millennia been considered as valuable sea vegetables. In the face of an ever-growing population, seaweeds are predicted to play an increasing role as a food source. Based on their fast growth, [6] global availability and suitability as food, they represent a viable possibility in providing food security [7].

Nowadays, 31–38% of the seaweed aquaculture biomass is directly used as food [8]. Polysaccharides extraction is the second largest application of seaweeds [8, 9] being commercially employed in food products due to their jellifying qualities, as food additives, other food supplements, and hydrocolloid compounds for medicines, nutraceuticals, and cosmetic products [8, 9]. Agar, alginate, and carrageenan are economically exploited [10, 11]. Seaweeds are also used in applications including animal feed [12], fertilizers, bioplastics, and biofuel [8, 9].

Currently, most of all commercial seaweed comes from aquaculture rather than wild harvest [13]. Although the seaweed market is still emerging in many parts of the planet, the established market is already considerable [14]. To support growing seaweed market resource demands while ensuring high-quality seaweed products, an expansion of seaweed aquaculture is required [11]. This expansion holds a multitude of benefits. It offers the opportunity to increase an economically potent market while protecting wild populations from overexploitation through harvesting [11]; it supports a sustainable market [15] while algae-based products have the potential to replace unsustainable products [8, 9] and food production methods with sustainable alternatives [16].

This chapter elaborates upon the current state of seaweed aquaculture globally and cultivation methods that are commonly applied. Furthermore, it discusses the potential benefits and drawbacks of seaweed aquaculture regarding an emerging blue economy and its wide-ranging effects on society and the environment. Lastly, the ecosystem services and climate change adaptation potential of seaweed cultivation are discussed.

2. Seaweed aquaculture: current status

2.1 Global seaweed aquaculture

Seaweeds have vast applications for human benefit, with their full potential still being explored. In 2020, the total production of world seaweed aquaculture grew by half a million tons, up by 1.4% from 34.6 million tons of fresh weight (FW) in 2019 [17]. Over 99% of the production is grown by various methods in Asia. Typically, only five major countries (China, Indonesia, the Philippines, Korea, and Japan) produce over 97% of seaweed globally [18]. Amounting to more than 32 million tons (Mt) in 2017, seaweed production is responsible for a large proportion of the global aquaculture’s liveweight, only topped by freshwater fish [8, 13]. Within the global aquaculture production, the two most cultivated species groups in terms of fresh weight are seaweeds: Japanese kelp (family Laminariaceae) and Eucheuma spp. [8].

Since seaweeds have been a part of the cuisine of many Asian countries for about for hundreds of years, it is not surprising that seaweed production is dominated by Asian countries [19] and 99% of seaweed aquaculture is situated in Asia [8]. In contrast, in Europe and the Americas, seaweeds are still mostly harvested from nature [7, 20, 21]. Outside of Asia, only Zanzibar’s and Chile’s aquacultures produce significant amounts of seaweed on a global scale [7]. In Europe, only 1% of the produced seaweed biomass consists of aquaculture, of which Norway, Denmark, and Spain are at the forefront of the number of companies [20]. Figure 1 presents the major seaweed aquaculture species and their uses [17].

Figure 1.

Major seaweed aquaculture species and their uses.

2.2 Seaweed aquaculture cultivation methods

Cultivation methods can be characterized by their location, approach, farming process, or cultivation technique [7, 22, 23]. Some of these (Figure 2) will be discussed here with special regard to their sustainability.

Figure 2.

Cultivation methods assessment based on several parameters (location, approach, farming process, or cultivation technique).

Offshore and nearshore cultivation are terms that differentiate between farms far and close to the coast, although an official legal definition does not exist [22]. Nearshore aquaculture is the most common seaweed farming method and has the benefits of needing little labor and seaweeds being quite sheltered against harsh conditions of the open water [22]. The environmental upside of this cultivation technique is that it can take up nutrients from agricultural effluent [24], acting as a nutrient bio-extraction system [19]. For large seaweed farms, interest in offshore cultivation has been growing [22]. It is slightly more labor-intensive than nearshore cultivation but still inexpensive [22]. However, seaweeds are exposed to harsh conditions offshore and are faced with several other difficulties related to epiphytes, making the method only suitable for certain seaweed species [22]. The problem with epiphytes is that they compete with macroalgae for space, nutrients, light, etc., causing detachment of host tissue. It can be environmentally friendly, but the downside is that the transport to and from the cultivation system adds to the energy usage [22].

In contrast to the previous two methods, onshore cultivation takes place in a closed or semi-closed system. This enables much control over abiotic factors, like seawater in- and outflow, nutrients, light, pH, CO₂, and salinity, and protects them from harsh environmental conditions like winds and waves [22, 25]. Although expensive, it enables consistent production, which makes it attractive for commercial large-scale production, especially for high-value product extraction [22, 25]. Besides, it is suitable for a wide range of different species that would be difficult to cultivate otherwise [25]. A specific form of onshore land-based cultivation is Saline Aquaculture, which makes use of saline groundwater [22]. Earthen or plastic-lined ponds, raceways, and tanks are some of the farming systems used in this method. Some advantages of marine algae culture include the ability to use existing agricultural farms where saline water is available, which is less constrained by the need for additional resources than farming in the sea. Another advantage of cultivating marine algae in island saline water (ISW) is that it can provide an additional source of income and raw marine algae for the aquaculture seaweed industry and has a lower investment than offshore and nearshore farming [22], which could make it an interesting option for lower-income countries. Concerning sustainability, there are both advantages and disadvantages to onshore aquaculture of seaweeds. Since the effluent is controlled, the impact of onshore cultivation on its physical environment can be minimized, even when nutrients are added [25]. Additionally, because onshore systems are three-dimensional, they are more efficient in terms of area than classic offshore cultivation [25]. However, onshore cultivation comes with significant energy requirements [25]. Moreover, in contrast to offshore cultivation, it is located on land and thus lacks the advantage of offshore cultivation of not competing for arable land [22].

Especially of interest for conserving the environment is integrated multi-trophic aquaculture (IMTA). This cultivation method uses species of different trophic levels [26]. More specifically, it combines waste or nutrient-producing aquaculture with extractive species like seaweeds, thus mitigating the impact of the system on its environment [19, 26]. For example, in Portugal, sustainable production of seaweed (Algaplus company) uses this IMTA concept, farming seaweeds in proximity to several species at different trophic levels, allowing the reduction of aquaculture wastes [27]. IMTA is practiced in a controlled environment on land, with organic certification for quality, traceability, stability of supply, and a small carbon footprint. Although it still faces some challenges regarding contaminants and complexity, it is a promising “ecological approach to aquaculture” and is part of the EU’s Blue Growth Strategy [26]. In general, seaweeds are cultivated in one or multiple-step farming systems [28]. Clonal species, such as Gracilaria and Kappaphycus (Rhodophyta), can be fragmented vegetatively and propagated directly for growth in culture systems. This can be done at different scales, moving from intensive on-land tanks or ponds to extensive open sea culture systems using long lines or rafts. On the other hand, propagation of unitary seaweeds such as kelp for industrial cultivation requires a hatchery/nursery. The different cultivation systems have been thoroughly tested experimentally, but the most commercially successful systems have been those that culture seaweeds at sea due to lower operational and capital costs [7].

3. Seaweed aquaculture: a future road to blue economy?

In recent years, the concept of the ‘blue economy’ has attracted the attention of policymakers, managers, and scientists alike. Since the introduction of the term to protect the global seas and their resources while supporting the human population [20], current definitions of blue economy have progressed to encompass a vast array of components far beyond its original scope. For example, according to the United Nations, blue economy is “a long-term strategy aimed at supporting sustainable economic growth through oceans-related sectors and activities, while improving human well-being and social equity and preserving the environment” [29]. According to the World Bank, the blue economy is the “sustainable use of ocean resources for economic growth, improved livelihoods, and jobs while preserving the health of ocean ecosystem” [30]. European Commission defines it as “All economic activities related to oceans, seas and coasts. It covers a wide range of interlinked established and emerging sectors” [31]. Nowadays, blue economy describes an approach to the immediate and long-term development and growth of a sustainable economy [32, 33], which promotes human health and wealth, food security, and the conservation of the marine environment and its resources [33, 34, 35]. Forms of blue economy have been applied in traditional management for millennia [36], as exemplified by Keen et al. for Pacific islanders [33]. This concept is also closely related to the term “phyconomy,” which is hereby coined to describe a general concept that embraces large-scale, sustainable seaweed farming for economic benefit in coastal waters. As an emerging sector that holds the potential for vast economic growth in upcoming decades [22], the aquaculture cultivation of seaweeds is often associated with the concept of blue economy. This association is reflected in notions such as the “blue dimensions of aquaculture” [37], “blue bioeconomy” [13, 20], or “phyco-economy” (a concept of the industrialized and sustainable cultivation of seaweeds) [38]; which already tie seaweed aquaculture to the blue economy. In the following paragraphs, the potential of seaweed aquaculture to the blue economy will be elaborated upon, in respect to aims of blue economy: human health and wealth, food security, promotion of social factors as well as the conservation of the marine environment and resources.

3.1 Economy

The industry has a large potential for fast expansion, as initial investments are comparatively low (depending on species, technique, and location), while returns are high [33]. The time until settlement, however, is very short: the period between planting and the first harvest of seaweeds spans less than 2 months [11, 33].

Additionally, areas suited for seaweed aquacultures amount to 48 million km², over 99% of which are currently unused for the purpose [34, 39, 40]. Less than a third of the 132 countries with suitable areas currently engage in seaweed cultivation [34, 39]. Seaweed farming thus has a high potential for expansion of the sector, which is supported by a growing relevance of seaweed products [22], while low financial thresholds offer an opportunity for economic development and the creation of jobs in low-income countries. It is worth mentioning that previous studies that have identified “high opportunity marine ecoregions” (HOMEs) for the development of seaweed aquaculture in consideration of socio-economic and environmental factors have determined that most HOMEs border wealthy countries rather than low-income countries [15]. Again, this, if not considered, could further add to global inequalities.

Seaweed-based products have several valuable economic applications, including seaweeds for consumption, dried seaweed, and seaweed extracts, as well as products based on these applications. Fresh or dried seaweeds for human consumption, hereafter referred to as edible seaweeds, have a higher market value than products for extraction purposes [10]. Edible seaweeds currently render >3 billion US$ annually [41]. Extracted algal polysaccharides (namely fucoidan, alginate, ascophyllan, laminarin, porphyrans, agar, carrageenans, and ulvans) have high market value already and are expected to become increasingly demanded and thus economically prized [33]. Agar and carrageenan (both retrieved from Rhodophyta, red seaweeds) [42] as well as alginate (retrieved from Phaeophyceae, brown seaweeds) are presently the most demanded algal polysaccharides [33, 43]. By 2024 [42, 44], agar, carrageenan, and alginate are expected to reach a market value of 1 billion US$, with growth continuing until 2025 [33]. On the global market, a diversion between market value and demand is regionally present: in several Asian countries, edible seaweeds are highly demanded for consumption, while in wealthy westernized countries, the market offers a large niche for seaweed extract products [10]. It is also relevant to note that while the interest and approximated demand in the use of seaweeds for biofuel is growing, its economic value is relatively low [7].

Recent data on the growth of the sector is ambiguous. Seaweed aquaculture currently provides annual revenues of around 6 billion US$ [41, 45], and with a threefold increase in value in the past 100 years as well as continued growth until the last decade [10], seaweed cultivation is regarded as a promising economic sector by a multitude of publications [22]. A recent study has found that in the past 10 years, a 150% increase in “algae-producing companies” has taken place [20]. However, recent reports have met this enthusiasm with doubt. Buschmann et al. [7] have regarded the potential of the seaweed aquaculture sector as “larger than its actual scale,” historically as well as at current. In a 2011 report, the Food and Agriculture Organization (FAO) estimated the annual value of seaweed at around 7 billion US$, which indicates a 1 billion US$ decrease between 2011 and 2018 [41, 46]. Moreover, in 2020, the FAO illustrated that the production of cultivated algae, a majority of which are seaweeds, has encountered low growth in recent years, with a decrease of 0.7% in 2018 [13]. While production trends do not necessarily reflect the market, they support Buschmann et al. [7] in their reservation about the potential of the sector at its development. Additionally, repeated mentioning of “hurdles,” such as unclear legislation, protocols, and guidelines, and contradiction within the aim of the blue economy itself, have been brought forth in recent publications on the subject [7]. Still, most studies conclude that seaweed aquaculture has a high potential within the scope of the blue economy once current hurdles are overcome [7, 20].

3.2 Human health and wealth

An expansion of the seaweed aquaculture industry also offers employment and a linked increase in socio-economic wealth in low-income countries, as has already been recorded in several such countries [7, 14, 22, 47]. The industry also offers safe work conditions as the aquaculture is located in the shallow intertidal [11]. Ferdouse et al. [34] have pointed out that seaweed aquaculture has the potential to especially support and empower women in areas where they have thus far had little independence, which can support their families with their own income [34]. However, this argument of moving toward gender equality should not be treated lightly, and its use as a “catchphrase” should be avoided, as the curation of jobs does not have a direct positive effect on minorities or currently oppressed groups. The same paper also included children in this consideration of safe access to the aquaculture industries [11]. Again, caution is urged, and a need for the provision of support and guidance presents itself. An increased cultivation of edible algae, which currently represents around 40% of the worldwide seaweed production, has the potential to reduce food shortage [7, 33]. Again, this especially applies in low-income countries, as it is a cheap and efficient alternative to land-based agriculture food production. Seaweeds, often also referred to as sea vegetables, have the potential to significantly add to the global protein supply within the next decade [7]. Lastly, an interconnection inside the formation interconnection between non-market value ecosystem services and human welfare, which adds to the objective of the blue economy, has been established [7].

3.3 Conservation of the marine environment and resources

Seaweed’s aquaculture cultivation is frequently described as sustainable and environmentally friendly and thus fits well into the framework of the blue economy. This characteristic is based on several factors. Firstly, unlike terrestrial agriculture, the farming of seaweeds does not utilize any fertilizer and pesticides [34] or feed and other organic waste compared to fish monoculture [6, 48]. As such, it does not produce nutrient-rich, and consequently, eutrophication causes discharges. On the contrary, seaweeds absorb excessive nutrients such as nitrogen, carbon, and phosphorus from the water column and reduce associated eutrophication [6, 19, 49]. Furthermore, wastewater discharges can be filled with heavy metals and other pollutants, and to prevent these compounds from entering the food chain, seaweeds, with their biosorption properties, can be taken advantage of [50]. Due to the macromolecules (mainly polysaccharides) in the cell walls, seaweeds can bind metal ions and heavy metals such as arsenic or lead [50, 51]. However, seaweeds that have bio-accumulated a high concentration of heavy metals need to be removed so they do not endanger the food chain [52] and cannot be used for human consumption [51]. Seaweed aquacultures can accordingly be a tool in bioremediation and reduce eutrophication [15, 53]. It is relevant to note that the bioremediation efficiency differs among species [54]. The energy transfer from dissolved nutrients to seaweed biomass also contributes to an increase in food availability for associated species [55]. Beyond that, as mentioned previously, seaweed cultivation can be linked to fish raising in integrated multi-trophic aquaculture (IMTAs) [6, 48]. In IMTAs, the excess nutrient discharge (organic and inorganic substances) from fish production systems can be absorbed and utilized by seaweeds, which act as biofilters and turn into biomass production [6, 19, 56, 57, 58]. Through creating a link between the rearing of live animals and seaweeds, the blue economy is supported beyond the direct extent of seaweed aquaculture. Instead, the seafood and fish aquaculture sectors, which are heavily criticized for their environmental impact while holding the key to providing sufficient seafood and conserving wild fish populations, can be supported [59, 60]. Additionally, by replacing wild fish with seaweed components in fish feed [61, 62], wild fish populations can be protected.

Aquaculture cultivation of seaweed also forms a temporary habitat for other potentially vulnerable species [20, 63, 64]. Increases in biodiversity of herbivores as well as other species attracted to the complex habitat such as fish and invertebrates are commonly observed [6, 63]. Seaweed farms can also act as nursing habitats [65], as exemplified by Hughes et al. [66]. However, these positive effects on biodiversity are limited to the period until harvest [63]. Apart from habitat provision, the physical structure of seaweed habitats presents several beneficial services to the surrounding ecosystems [34]. It depletes waves and currents of their energy before meeting the coast and concurrently prevents erosion [63, 67].

According to Choudhary et al., commercial seaweed cultivation can aid in the conservation and recovery from overexploitation of affected macroalgae species, as they are released from unsustainable harvesting pressure. An example is Gracilaria sp. (Rhodophyta), which was impacted by unsustainable harvesting in Chile and has been released of this pressure [59, 60].

Similarly, commercial species such as Laminaria hyperborea (Ochrophyta, Phaeophyceae) in Norway are currently harvested by specialized trawling gear [6]. The harvest of seaweeds by trawling implies the removal of benthic flora and fauna as well as the destruction of habitats [6]. Expanding the cultivation of such species offers the potential to meet the increasing demand for the product [6] and release affected ecosystems from the pressure of trawling.

Seaweed aquaculture offers a variety of opportunities to support the adjacent ecosystems, the effects of which are often described as ecosystem services. As such, it generates an extended non-market value [7]. Ecosystem services are variable and include supporting, regulating, and provisioning services [49]. While the value of these non-market-value services is difficult to estimate, attaching a monetary value to these services has the potential to further enhance the economic value of seaweed aquaculture beyond their marketable value [68].

A comprehensive analysis considering where each service of seaweed cultivation can be placed within the paradigm of ecosystem services is provided by Hasselström et al. [49].

However, several questions arise regarding the potential negative effects of seaweed aquaculture on the ecosystem. Does future commercialized extensive cultures of seaweeds pose a risk to the genetic variation of wild populations? Could they mirror land-based agricultural monocultures in their negative effects on the environment?

Firstly, the environmental and physical impacts of seaweed aquaculture systems need to be considered. Depending on the species and system, the mariculture of seaweeds can require the clearing of an area from rocks or species growing in the area. When floating structures are used, they can cause shading of the adjacent water column (Figure 3). All systems can cause a change in sedimentation, flow regime, and other disturbances through the swaying of the seaweeds or even indirectly through an altered species community surrounding the systems [63]. In land-based systems, problems are fewer. A main issue is the use of space for pond creation [22]. Additionally, seawater must be supplied and then discharged. However, the discharge has few excess nutrients, and associated problems are expected to be minor [63]. Spatial planning can be crucial here, and assigning areas for aquacultures can cause or be hindered by conflicts of interest.

Figure 3.

Chondrus crispus aquaculture floating system.

A vast proportion of cultured species is not native to the region of cultivation, such as the red seaweed Gracilaria vermiculophylla (formerly Agarophyton vermiculophyllum), native from Japan, that has invaded estuaries throughout the whole world, and the brown seaweed Sargassum muticum (Phaeophyceae), native seaweed from Japan and China, currently widespread along the European shoreline [69]. These non-native species have historically caused invasions in the range of introduction, where they can compete with or even outcompete native species [70]. As invasive species become dominant, they can alter the local species assemblage [70] and influence the functioning and stability of the ecosystem [6]. Furthermore, the introduction of seaweeds to an area for aquaculture increases the likelihood of unintentional introduction of non-indigenous “hitchhiker” species, including pathogens [22]. All of these non-native species can spread easily over short and also longer distances due to the open and dispersive nature of the ocean.

Next to non-native species, the so-called crop-to-wild gene flow negatively affects local seaweed populations. Selective breeding of the cultivars used for aquaculture crops is practiced to enhance beneficial traits including biomass, growth rate [6], or disease resistance [19]. This practice tends to reduce the genetic variability and associated evolutionary adaptability of the cultivated seaweed [19]. Again, the dispersive and open nature of marine systems allows for gene flow between wild and cultivated crops, through which the selected alleles can become established in wild populations [70]. The resulting genetic depletion can leave the native population vulnerable, as its ability to adapt to a changing environment is decreased [6, 63, 71].

4. Seaweed aquaculture and climate change adaptation

While seaweed aquaculture carries great potential as a sector in the blue economy based on its primarily positive impacts on the above-described factors, it exceeds the current definition of blue economy by the United Nations. Large-scaled seaweed cultivation can also positively affect climate change scenarios and allow for climate change adaptation. This fact scenario will be discussed here.

Currently, increased emissions of the acidic gas carbon dioxide induce an increase of CO₂ in the atmosphere and oceans. This increase leads to the acidification of global oceans. Ocean acidification is especially harmful to calcified seaweeds (such as Corallinaceae) and animals with calcified body structures, as the decreased pH dissolves these structures [72]. Seaweeds are autotrophic plants and, as such, perform photosynthesis. Through this process, they transform CO₂ into energy [73, 74]. Seaweeds continuously take up CO₂ and in turn reduce its concentration in the oceans [45, 75], which consequently increases the pH of seawater and reduces ocean acidification [39, 76]. As a consequence, seaweed beds, including aquacultures, provide refuge to vulnerable calcifiers and other species [72, 75, 77]. Seaweed production through cultivation is crucial for the capture of CO₂ from the atmosphere [73]. The use of seaweed as a CO₂ sink provides one way to extend blue carbon strategies [78, 79]. Recent studies found that macroalgae detritus has a high potential for carbon sequestration [80, 81]. Unlike other ecosystems that provide plants, like seagrass, seaweed does not form sediments around their holdfasts due to the hard nature of the substrate they grow on [80, 82]. However, seaweed detritus is transported to recipient sites, where they are deposited along with the absorbed atmospheric carbon [80]. Such recipient sites were recently found to extend coastal areas by up to 5000 km and include the deep seas [83]. In offshore and deep areas, limited human influence and wave action reduce the probability of the carbon returning to the atmosphere and instead remain sunk [82]. Here, carbon provides an important food source, and on the other hand, it is sunk in the sediments of the deep coastal benthic food web [81, 84]. It has been estimated that over half of the green carbon capture, thus the capture of CO₂ through terrestrial and marine systems, is through the marine realm [81]. Mashoreng et al. [85] have found that an average of 57.64 tons CO₂ ha⁻¹ yr⁻¹ in ocean-based seaweed aquacultures and 12.38 tons CO₂ ha⁻¹ yr⁻¹ in land-based aquacultures could be sequestered. In strategies toward blue carbon capture, it should thus be considered that land-based pond systems offer less potential for blue carbon capture [85]. Additionally, it was found that seaweeds at different developmental stages display different carbon sequestration potentials [86]. Fakhraini et al. [86] determined that in research aimed at analyzing carbon sequestration potential on seaweed Kappaphycus striatus adult plants have 32.78% more potential than young plants. While the potential of seaweeds in climate change and their application in “Blue carbon farming” is vast, it is important to consider the spatial planning of seaweed farms. Here, it is especially important to assess and determine the minimum and maximum extent of the farms to ensure efficiency and prevent depletion of coastal carbon. A depletion of carbon could affect other ecosystems, such as seagrass meadows, which in turn provide habitat and resources to other organisms [75]. While the use of seaweed aquacultures in the blue carbon framework is still relatively undeveloped, and knowledge gaps are present, it has been determined to play an imperative role in carbon capture [87].

While transforming CO₂ into energy, seaweeds produce O₂. Another effect of climate change is eutrophication, a removal or lack of oxygen predominantly from coastal areas [88]. Eutrophication is the enrichment of water with nutrients such as minerals, nitrogen, and phosphorus-containing materials. This frequently leads to the unwanted and excessive growth of aquatic or marine plants (algae blooms). Eutrophication can occur naturally, but it can also be accelerated by allowing water rich in dissolved fertilizers to seep into nearby lakes and streams or by the introduction of sewage effluent into rivers and coastal waters. Seaweeds can be used to reduce the nitrogen and phosphorus content of effluents from sewage treatment. Many seaweeds prefer taking up ammonium as the form of nitrogen for their growth, and ammonium is the prevalent form of nitrogen in most domestic and agricultural wastewater. Seaweeds add O₂ to the ecosystem and can help mitigate this issue. Seaweed aquaculture has the potential to act as a supplementary force to wild seaweed populations in their ability to perform such services [75]. Additionally, seaweeds grown in coastal aquacultures have the potential to support other climate change adaptations—strategies to mitigate the effects of climate change (events) on the planet and human societies [75, 89].

Seaweed aquaculture, however, also has less direct and apparent potential in climate change mitigation. Seaweed can be used directly as a replacement for traditional fossil fuels. Several species of seaweeds accumulate high levels of carbohydrates, which are suitable as substrates for microbial conversion processes, e.g., for the production of bioethanol, biobutanol as biofuels, or other desirable chemicals with an attractive high product value. Kelp species contain 50–60% carbohydrates of the dry weight, and cultivation techniques have been firmly established for the last 50 years. Moreover, kelp is cultivated in large quantities, providing an abundant and potential carbon-neutral renewable resource with the potential to reduce greenhouse gas (GHG) emissions and the man-made impact on climate change [90].

Another application of macroalgae is in agriculture, where they can be used to lower the discharge of pollutants by improving the soil and/or their use in animal feed [74]. The cattle business is among the major causes of methane (CH₄) emissions. Excessive methane emissions directly affect climate change, as they aggravate greenhouse warming [91]. A previous study found that with a 2% increase in the alga species Asparagopsis taxiformis (Rhodophyta) in cattle feed, methane emissions decreased by 99% [74]. In a study focused on the agricultural cultivation of sugarcane, Singh et al. also found that Kappaphycus (Rhodophyta) extract as a fertilizer has the potential to lower CO₂ emissions. It further increased the economic value of the product [92].

5. Future perspectives

This emerging sector holds great potential—if well planned. Currently, the potential of seaweed aquaculture is not yet fully realized, and authors have pointed out “hurdles” that need to be overcome to do so [7, 21]. A lack of up-to-date guidelines and laws surrounding seaweed cultivation is present, and the provision of such is recommended. An example of this issue is represented by the currently poorly regulated genetic profile of seaweed cultivars 10, 11, 63, 69, 70. As the gene flow between cultivated and wild seaweeds cannot be prevented, well-informed regulations that determine the genetic diversity of cultivars should be implemented [7, 70]. However, currently, knowledge of this topic is limited [93]. On another note, spatial planning and the effects of implementing aquaculture have highly localized effects, and guidelines and recommendations for an approach to assessing and avoiding stressors could be advantageous [75, 94]. Such plans should also target currently under-addressed topics such as an excessive uptake of nutrients and altered flow regimes, which could negatively impact surrounding ecosystems. At this point in time, a lack of studies assessing such interactions is apparent [75].

Previous analyses have considered the potential of blue economy. To do so, the tools of quantification and monetizing the potential damages and benefits, such as economic values and prices paid by society and ecosystems, have been applied. Such benefits and externalities to the natural environment and human society can be measured, and a monetary value can be assigned according to cost-benefit analyses (CBA), which can serve as a tool in this process [70]. However, CBAs are not always objective, and results differ between studies [95]. Another approach to developing a critical step-by-step approach based in a SWOT (strength-weakness-opportunity-threat) analysis based on human risks, experienced environmental impacts and costs, constraints in economic growth, and feasibility of the aquaculture project [40].

There is a need for the promotion and growth of the sector globally and the overcoming of conflicts of interest presents. In particular, the promotion of partnerships between academics, companies, and communities to develop communication and technology for the purpose of creating long-term economic impacts is relevant. Moreover, there is a need for the expansion of the seaweed market. Government authorities and governmental capacities are key players in taking charge of expanding the sector [21].

6. Conclusions

Seaweed aquaculture offers a range of benefits to society, the environment, and the sustainable development of the economy. Under consideration of the overexploitation of wild seaweeds and an increasing interest in and application of seaweeds, it appears that aquaculture cultivation holds the future of commercial seaweed production to continue to meet the demand. However, at this point, only a fraction of the suitable areas for seaweed cultivation are utilized. Seaweed aquaculture has a large potential to grow, physically and as a market, if increased attention, research, and investment are devoted.

Seaweeds can be cultivated in the marine environment, nearshore, and offshore, as well as in saline land-based ponds. All methods are found to be viable, and none presents itself as highly favorable or disadvantageous. While the techniques of seaweed aquaculture systems, especially the integrated multi-trophic aquaculture systems (IMTAs), can be improved upon, they can support sustainability and a blue economy.

The potential relevance of seaweed aquaculture in the blue economy has become apparent. The sector can add to all components of the blue economy: economic growth, conservation, and social factors such as human wealth and health. Yet, several negative aspects, which especially affect the surrounding environments, need to be considered and overcome.

Seaweed aquaculture was also found to extend beyond the scope of the blue economy and reach into land and ocean-spanning climate change adaptation. Expanded seaweed aquaculture can provide services to reduce the effects of climate change and associated events, such as increased storm intensity and frequency, eutrophication, and ocean acidification. Furthermore, seaweed aquaculture can support the blue carbon framework due to its capacity for carbon sequestration. The use of seaweed aquaculture in counteracting the effects of climate change and correlated events is still in its infancy and should be further explored.

Acknowledgments

This research was co-financed by the project MENU—Marine Macroalgae: Alternative recipes for a daily nutritional diet (FA_05_2017_011), funded by the Blue Fund under Public Notice No. 5-Blue Biotechnology. João Cotas thanks the European Regional Development Fund through the Interreg Atlantic Area Program under the project NASPA (EAPA_451/2016). Diana Pacheco, thanks to 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). Alina Hillinger and Kay Ihle would like to thank IMBRSea—The International Master of Science in Marine Biological Resources. Ana M. M. Gonçalves acknowledges the University of Coimbra for the contract IT057-18-7253.

Conflict of interest

The authors declare no conflict of interest.