IMTA), and the Possibility for Its Optimization

SJÄLVSTÄNDIGT ARBETE I MARINBIOLOGI 15hp, VT 2020 cd

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Concerning the Viability of Offshore Integrated Multi-Trophic Aquaculture (IMTA), and the Possibility for its Optimization.

Författare: Leo Näsström Handledare: Michael Tedengren, DEEP

Angående möjligheten för utomskärs integrerad multi-trofiskt vattenbruk och dess potentiella optimering.

Sammanfattning

Ett stagnerat globalt fiske har lett till en snabb utökning av vattenbruket för att tillgodose den globala marknaden. Traditionellt vattenbruk har i västvärlden kännetecknats av monospecifika odlingar, ofta med mycket grav påverkan på sin omnejd. Ett återupptäckt alternativ till denna i längden ohållbara tappning av vattenbruk har därför växt fram. Integrerad multi-trofiskt vattenbruk (IMTA) är en teknik som, genom att odla organismer från flera trofiska nivåer tillsammans, kan minska utsläppen och öka produktiviteten hos en odling. En växande global befolkningen kommer dock leda till ökande konflikter mellan kustnära vattenbruk och intressenter såsom industrier, myndigheter och privatpersoner. Då vattenbruket fortsätter att växa skulle en lösning på dessa konflikter vara att rikta dess expansion mot det öppna havet. Frågan är då om IMTA vore effektivt utomskärs och hur det i så fall skulle kunna optimeras ur både produktions- och kostnadsperspektiv. Denna undersökning tyder på att en pelagial expansion skulle ge en positiv påverkan av de olika ekologiska, ekonomiska och infrastrukturella aspekter rörande utomskärs-IMTA. Dock kräver en sådan förflyttning omfattande förarbete i utvärdering av lämpliga lokaler. En analys av olika arter och dess egenskaper, monetära värde, tillika möjligheter att optimera systemet visar på att utomskärs IMTA är möjligt, men begränsas av ingenjörsmässiga faktorer.

Abstract

The stagnated global fishing has led to a fast expansion of aquaculture to meet the increasing global demand for seafood. Traditionally aquaculture in the western world has been defined as large monospecific cultures, often with grave implications on its surrounding environment. An alternative to the conventional and unsustainable method has thus been rediscovered and developed. Integrated Multi-Trophic Aquaculture (IMTA) is a technique that, by cultivating organisms of different trophic levels together, can decrease effluents and increase the productivity of a farm. Furthermore, the growing global population will lead to increasing conflicts between coastal aquaculture and other stakeholders such as industries, governments, and private citizens. Since aquaculture continues to grow, a possible solution to such conflicts could be an offshore expansion of aquaculture. However, whether an IMTA system still would be effective in an offshore setting is unclear. This is also the case regarding the possibility to optimize an offshore IMTA system concerning productivity and investment costs. The present article shows that a pelagic expansion of IMTA would positively affect the ecological, economical and infrastructural aspects regarding offshore IMTA compared to inshore IMTA. However, such a transposition would require comprehensive preparatory evaluations of suitable sites. An analysis of several species and their attributes, monetary value, and capability of optimizing the system indicates that offshore IMTA is possible but is limited by structural-engineering factors.

Introduction

The global demand for seafood and other marine products is on the rise and, due to a stagnated production in capture fisheries, this demand cannot be met by capture fisheries alone. This has led to the rapid development of aquaculture to mitigate the limited supply and meet the increasing demand for seafood and marine products. In 2016, aquaculture supplied about half of the total aquatic produce, excluding aquatic mammals, caimans, crocodiles, alligators, aquatic plants, and seaweed (FAO, 2018). Aquaculture´s production and the corresponding global consumption, both in total and per capita, have been steady; With, as of 2016, China as the major producer of farmed fish. Further followed by, with no internal order: India, Indonesia, Viet Nam, Bangladesh, Egypt, and Norway. By 2016, China and Indonesia were the largest producers of aquatic plants and seaweeds (FAO, 2018). An interesting observation is the absence of producers from the Americas and Europe, the exception being Norway. However, these statistics show the production from all types of aquaculture and do not discriminate between monospecific aquaculture or other techniques of polyculture such as Integrated Multi-Trophic Aquaculture (IMTA).

IMTA is a method of cultivating different species from different trophic levels together. The IMTA system is usually composed of a carnivorous finfish species together with extractive species such as macroalgae and bivalves. IMTA thus allows for the reduction of unwanted byproducts from the intensive fed aquaculture, mainly: Particulate Organic Matter, POM: e.g. fecal matter and disregarded food pellets, and dissolved nutrients e.g. ammonium, (e.g. Alexander et al., 2016; Chopin et al., 2004, 2001; Troell et al., 1997). Thereby, IMTA allows a farmer to generate more product/profit per invested dollar, and to significantly reduce the effect of the farm upon the surrounding environment (Chopin et al., 2001), as well as internalizing the environmental costs making the industry more economically sustainable for the society as a whole (Folke et al., 1994). By using IMTA the farmer also diversifies the income of the aquaculture farm viz. providing the farm with uncorrelated sources of income. Thus, allowing a farm to be more resilient against losses of production/income, caused by factors such as a market value drop of a species, disease and unfavorable weather causing a reduced amount of product (Ridler et al., 2007; Troell et al., 2009). Since IMTA is a system built on combinations of different species who have different innate abilities, the efficiency of the whole system depends on what species the combination is constituted by and the ratios therein (Lamprianidou et al., 2015). The whole IMTA system´s bioremediation efficiency can, in addition to the ratios and combinations of species, be optimized by altering the values related to the practices surrounding the system, such as the density of the extractive species grown or its harvesting frequency (Buck and Buchholz, 2004; Lamprianidou et al., 2015).

In a study of the European public’s knowledge and preferences of aquaculture and consumerism Alexander (2016) found that out of the 2520 European respondents in five different countries, a majority did not know what integrated aquaculture was. However, when having integrated aquaculture explained to them a majority was positive when asked whether they thought it would have potentially good effects on issues surrounding aquaculture, e.g.

food production, sustainability, environmental impact, among others (Alexander et al., 2016). This suggests a positive attitude for integrated aquaculture of the European public that could suggest a great market for environmentally friendly products from IMTA systems.

The aquaculture that has been developed and practiced the most in recent history is characterized to be inland pond systems or inshore cages by the coasts (Buck et al., 2018). This has proven to become a factor of conflict among stakeholders competing for space for aquaculture practices, other industries in need of land for expansion, and cultural institutions consequently deteriorating the public perception of aquaculture. These conflicts, the fact that there are unexploited areas offshore, and the potentially reduced environmental impact, have driven the development of offshore aquacultures and a call by the FAO for further expansion of aquaculture into the ocean (Buck et al., 2018; Kapetsky et al., 2013). The EU commission have identified the heavy spatial competition both on the coastlines and offshore but have assessed that with proper preparation and identification of the offshore sites optimal for aquaculture, the spatial competition offshore could be overcome and are thus also advocating for offshore aquaculture development (“EUR-Lex - 52013DC0229 - EN - EUR-Lex,” 2013).

Aquaculture thus seems to be bound to expand offshore (e.g. Buck et al., 2018; Buck and Buchholz, 2004; Kapetsky et al., 2013; Potts et al., 2012; Troell et al., 2009) especially in areas that already experience a high population density and conflicts over land-use. Governmental bodies might edict policies to drive the transposition, as the instance of the EU commissions strategy guidelines (“EUR-Lex - 52013DC0229 - EN - EUR-Lex,” 2013). Although, is the IMTA system feasible for offshore aquaculture? How efficient would IMTA be in a high energy environment? And how could it be set up to be energy-optimized? In this present study, these questions will be analyzed by firstly examining the current literature and determine the current status of IMTA and then apply the concepts to an offshore environment.

Method

In the present study, peer-reviewed literature found through Google Scholar and Web of Science has been analyzed. The main search-words used were `ÌMTA Integrated Multi- Trophic Aquaculture´´ alone or with complementary and specifying search-words such as ``Bivalves´´, ``Holothurian´´, `Àlgae´´ / ``Macroalgae´´ and `Èchinoids´´. Furthermore, sources found in the references of other review articles on the subject were also used. When concerning data of capture fisheries, aquaculture, and the global markets, the Food and Agriculture Organization of the United Nations (FAO) was the primary source of data. Analysis

In the following section the different aspects and considerations of IMTA generally and offshore IMTA specifically will be analyzed. First, the technical details, problems, and economic aspects will be deliberated. The latter part will concern specific species´ and genus´ potential to be included in an IMTA system and the different aspects of those to consider.

IMTA and the open sea

The innate spatial competition of inshore and inland aquaculture against a constantly growing coastal population allows for the favorable expansion of aquaculture offshore. However, to be able to develop IMTA offshore one must consider very different environmental factors than those relevant for development in more coastal areas. In this review, the definition for ‘‘Offshore’’ by Jackson and Drumm´s (2010) will be used. This definition has also been adopted by the FAO (Kapetsky et al., 2013) and other authors (Ferreira et al., 2014). The definition is as follows: “In general Offshore Aquaculture may be defined as taking place in the open sea with significant exposure to wind and wave action where there is a requirement for equipment and servicing vessels to survive and operate in severe sea conditions from time to time. The issue of distance from the coast or a safe harbor or shore base is often but not always a factor.” (Jackson and Drumm, 2010). The definition itself states operational difficulties that need to be considered. This, along with other factors, prerequisites, potentials, and limitations of offshore IMTA will be processed next.

The competition and conflicts among stakeholders along the coastlines are considerable, making the move offshore a possible way to reduce and overcome conflicts and spatial disputes with other spatially requiring establishments, such as hotels, bathing-beaches or other aquaculture activities. In addition to conflicts caused by public concerns over environmental aspects (Troell et al., 2009). Offshore IMTA can likewise relieve the coastal area from exploitation altogether. One example is the issue of conversion of mangrove habitat into aquaculture ponds in coastal Bangladesh, where the mangroves have been attributed a vital role in Bangladesh´s resilience to Climate Change (Ahmed and Glaser, 2016). In that study, open water IMTA was thought to be one way to allow regeneration and protection for the mangroves and thus coastal populations.

Another factor in the incentive for offshore aquaculture and IMTA is that different abiotic conditions offshore can be favorable for IMTA, such as a higher turnover of water and thus resulting in a higher concentration of dissolved oxygen and high irradiance stimulating algal growth (Buck and Buchholz, 2004).

A high energy environment An offshore placement of a complex structure, such as an IMTA farm, has to be able to withstand a very harsh environment in which huge stress is put on the materials (Buck, 2007 p. 200). This calls for a flexible structure that can adapt to the conditions at hand, whether that is very turbid or calm, and still protect the cultures and providing them with the conditions they need for growth. Different systems and designs have been tested, one example is Buck and Buchholz´s (2004) Offshore Ring design for growing macroalgae. The system was based on a ring that was possible to build and attach pre-cultivated macroalgae culture lines before being towed out to sea. This designed thus allowed the algae to attach properly before being exposed to the harsh environment offshore where the system then could be anchored and tethered down by the tow- ship’s crew. At time of harvest, the procedure could then be reversed and the structure towed back to land (Buck and Buchholz, 2004).

An offshore placement for the IMTA would make it more difficult to cultivate benthic organism such as holothurians. To function as a part of the IMTA such benthic organisms thus needs to be suspended underneath the e.g. fish cages, in the area into which larger settling particles will fall. Yokoyama (2013) designed a technique of suspending holothurians

below finfish cages thus allowing the suspended holothurians to benefit unique advantages not enjoyed by benthic farmed specimens. By suspending the culture, one could avoid several disadvantages of the seafloor and surface, such as benthic predators preying on the holothurians or anoxic bottoms. As well as the low salinity, and high-temperature fluctuations of the sea surface (Yokoyama, 2013).

Nutrient fluxes and effluent emission. The complete bioremediation of phosphorus and nitrogen eutrophication is not the ultimate goal for integrated aquaculture (Chopin et al., 1999), IMTA farms will thus emit a certain level of nutrients depending on the composition of the system. An IMTA system will also exhibit seasonal nutrient and organic carbon emission fluxes (Fang et al., 2016) subjecting the surrounding environment to raised levels of nutrients depending on the cultured organisms’ temperature preferences and other factors such as sexual seasonality. Furthermore, offshore waters are generally less eutrophicated (Buck et al., 2018; Slater and Capone, 1987) which allows the surrounding system to buffer against said nutrient fluxes thus avoiding nutritional cascades that for instance can induce Harmful Algae Blooms (HABs). Although, this does not necessarily mean that offshore farms should be allowed to emit higher levels of nutrients than inshore, coastal farms (Chopin et al., 2012). Nevertheless, there is an issue concerning the environmental aspects of offshore farms that is the incentive of offshore farms to grow much larger than their coastal counterparts (further discussed under the subsection Offshore IMTA´s economics: is it viable?). A larger farm will emit higher amounts of nutritional effluents and will thus affect the proximate area to a larger extent than smaller farms. Although since the capability of offshore water to cope with large amounts of nutrients is higher, due to the generally more oligotrophic environment, it might still be favorable. However, an aquaculture farm will always have sedimentation occurring at some rate. An offshore farm located in deeper waters could thus affect ecosystems that are difficult to study or completely unknown deep-sea ecosystems.

Since the water offshore is generally less nutritious, it is also of higher quality. Clearer water provides a greater irradiance through the water column enabling a deeper cultivation zone for algal culture and thus protects the system to some degree from weather and waves (Troell et al., 2009). By cultivating the nutritional emitting species (i.e. finfish, bivalves, and, in some cases, holothurians) at a deeper depth, the risk of HABs decrease since the light availability decrease. Using natural or artificial upwelling zones, one can grow algae extractive species above the other species allowing them to enjoy the nutrient emission and thus stimulate the algae growth (Troell et al., 2009).

Ecological considerations in the offshore environment Pathogens

A problem for all aquaculture is the influence of fouling organisms and pathogens affecting both the organism itself and the human consuming the farmed organism. The pathogens in aquaculture have to a large extent, historically and in present times, been treated with antibiotics. Today the 15 major aquaculture producing countries use on average 15 compounds of antibiotics to treat their aquaculture (Lulijwa et al., 2018). IMTA has the natural ability, by biofiltration and decreased densities of each species of cultured organisms the potential to reduce the risk of a disease outbreak and thus reduce the ``need´´ for

antibiotics. A study by Pietrak et al. (2012) showed that Blue mussel (Mytilus edulis) has an ability to eliminate certain pathogens (in this case Renibacterium salmoninarum) in a cod farm, thus reducing the virality of the bacteria and the harm done by it. However, the authors also found that other bacteria, Vibrio anguillarum, accumulated in the pseudofeaces of the mussels. This could pose a potential risk if the sedimented pseudofeaces were to be resuspended by, for instance, a storm. Although, this was mainly a concern in shallow sites, and an offshore farm most likely will be located at a greater depth, thus reducing the risk of a resuspension event happening. Furthermore, if the farm were to be managed in such a way to keep the M. edulis feeding level below the pseudofeaces threshold (as discussed in the subsection Filter feeding bivalves in IMTA) the risk of the accumulation of the bacteria would decrease even further. Other than the risk of the cultivated organism suffering a disease, there is also the risk of the farm becoming a source of pathogens to the surrounding environment.

The pathogens discussed above mainly affect the cultured organisms and may be financially dangerous pathogens but cannot directly affect human health. However, human pathogens can be transferred from cultured organisms to the consumer through food and must therefore also be considered when evaluating a farm´s microbial community. When monitoring bacteria indicating the presence of human feces sourced from the major terrestrial discharges that are rivers and streams etc., Ahn et al. (2005) found that the concentration of these bacteria was multiple times higher in the surf- zone than compared to offshore sites. The sheer distance from the major sources of human pathogens, that is the coastal cities and rivers, to the offshore aquaculture farms is a major factor in reducing the risk of the presence of human pathogens in cultured organisms.

Biofouling

Another factor is fouling organisms covering the cultured organisms and equipment of the farm, thus reducing the efficiency of the farm (Buschmann et al., 1994; Fletcher, 1995). These fouling organisms could be everything from epiphytic algae to mussel larvae. To reduce the risk of fouling organisms’ influence, the farm’s biofiltration plays an important role in reducing the abundance of larvae in the waters. There is also a possibility to reduce the risk of epiphytes and other fouling organisms by placing a farm further from a possible source of these organisms. By maintaining the densities of the affected cultured organism, prominently the algae, epiphytes could be reduced, and finally, a systematic emergence of the cultivated organism has also shown to reduce epiphytes and contaminates (Fletcher, 1995). Herbivores Echinoids (sea urchins) could reduce epiphytic macroalgae (Sterling et al., 2016) and produce a valuable food product themselves since the gonads are highly valued in some many countries in Asia and South America. Another possible organism could be herbivorous gastropods which could provide a marketable product (Appukuttan et al., 1996) and reduce epiphytic growth (Osorio et al., 1993). Crustacean herbivores such as Isopoda and Amphipods could also be utilized to reduce the number of epiphytes, however, these do not produce a salable product.

Offshore IMTA´s economics: is it feasible? Offshore IMTA locations are, by definition, harder to reach and thus will be more expensive to operate, develop and maintain. The harsher environment will, as already discussed, also require higher quality materials and high structural complexity to be able to withstand the high energy environment both as a mechanic structure but also as a protective structure for the cultured organism. The higher base- level initial investment required will drive offshore

IMTA farms to be larger, thus allowing them to become more economically viable when comparing investment to yearly profit (Buck et al., 2018; Troell et al., 2009). Nevertheless, as IMTA is an expensive form of aquaculture, and offshore IMTA an expensive form of IMTA, one way to decrease expenses is to take advantage of other industries operating in the offshore theater. One way is by cost- and site-sharing, this mainly being cooperation with offshore energy establishments such as wind power plants. By cooperating, offshore aquaculture could decrease the initial investment and the continuous maintenance costs, as well as contributing to the importance of the site in the view of policymakers, thus giving more leverage when implementing regulations and policies protecting the area from disturbing activities such as boat traffic (Buck and Buchholz, 2004).

Although, even with cooperation with other industries and the cost reduction that follows, IMTA still is an expensive enterprise to develop, thus driving a financial skepticism towards it (Hughes and Black, 2016). In Europe, there is a lack of incentives, from the regulatory bodies, for the individual or company stakeholder, that, according to Hughes and Black (2016) contributes to the hesitation of individuals and companies to adopt the notion of IMTA. There has also been a development of increasing complexity of IMTA that the authors believe can be daunting for investors.

Optimizing an IMTA system

An IMTA system’s efficiency is dependent on its composition, with the main product usually being finfish but also other species produced are important. Thus, the different environmental- , economic-, and ecological aspects of potential IMTA composing species will fully have to be considered to optimize the system. In this section, these different aspects will be discussed.

Finfish The consumption of predatory finfish is very large, especially in the western countries (and EU) where the top four consumed fish are: tuna, cod, salmon, and Alaska pollock (Anonymous, 2019). These top predatory fish are expensive to breed but very valuable and sought after, making the aquaculture of these attractive for a farmer. Thus, a profitable IMTA probably will have a predatory finfish in the system as the fed species, however, the choice of finfish must be evaluated for economic value and environmental and dietary aspects considered since other species will rely on the same feed. A top predatory fish such as salmon will require larger amounts of higher trophic feed, and in turn excrete more nutrients than a lower trophic level fish such as a carp, making the carp more energy efficient than the salmon. However, most herbivores and lower trophic finfish that are desirable for aquaculture are freshwater species, these also represent the lion’s share of all farmed fish globally, but in marine systems, the most prominent species is the top predator the Atlantic Salmon (Salmo salar) (FAO, 2018).

Filter feeding bivalves in IMTA To determine the most appropriate bivalve to use as an extractive species in an IMTA system one has to assess the bivalves´ capability to filter and absorb particles from the water column (Troell & Norberg, 1998). For instance, M. edulis is a species frequently used in temperate aquaculture, by feeding on suspended particles that fall from the fed species (faeces and excess feed) and the surrounding environment the M. edulis reduces the particulate organic

matter, nitrogen and phosphorus in the regional area (Troell and Norberg, 1998). Troell and Norberg (1998) found that M. edulis had a linear response in its ability to capture suspended solid particles until a point when the mussels ingestion have become saturated and the mussels start extruding captured seston as pseudofeaces thus unable to reduce the particle loading in the water column. However, MacDonald et al (2011) found that M. edulis´s feeding activity was much higher when grown with S. salar, probably due to improved quality and quantity of the food available. These examples demonstrate the importance of relating the concentration and biomass of bivalvia per fed species biomass to optimize the reduction of nutrient wastes as well as the biomass production. Furthermore, they indicate that the systems are very complex and need to be considered as such.

The bivalve’s ability to absorb and reduce suspended particles in the water column to increase their growth is a key feature for bivalves as an extractive species in IMTA. However, the efficiency of the bivalves´ ability to reduce effluents has been described to be strongly correlated to the seston´s attributes such as the particles´ sizes, biochemical composition, and organic content (Irisarri et al., 2013). However, shellfish have in some cases shown only a small or no positive benefit in the market value and extractive abilities when grown in integration with finfish (Cheshuk et al., 2003; Cubillo et al., 2016; Taylor et al., 1992). However, some positive factors were shown. For instance, Taylor et al. (1992) found that, while the marketable value of the bivalves, the condition index, was not positively affected by the cultivating the bivalves close to the fish farm, the mortality and growth was actually affected by the distance to the fish farm. Cheshuk et al. (2003) on the other hand noted no large difference in the weight of the bivalves meat with the distance from the farm nor even a change in the particulate organic matter (POM) absorbed by the bivalves but argued instead (much like Troell and Norberg (1998)) that the mussel cultivation could have a more regional effect than local, resulting on a net loss of POM, nitrogen, and phosphorus. Cheshuk et al. (2003) also argued that for an effective bivalve integration to occur, the bivalves cultures site and design need to meet four criteria, which are: (1) the site shall have a high concentration of waste POM for extended periods of time, (2) Bivalves shall be cultured within 50 meters of the finfish cage and at least 5 meters deeper, thus intercepting falling particles from the finfish cage, (3) the particles shall be of such nature that the bivalves can filter and digest them, (4) the farm shall be placed at a location of a low ambient particle concentration. The latter one of these criteria is of special interest since offshore waters generally have lower particle concentration.

The genus Mytilus is commonly represented in studies of IMTA and other integrated aquaculture systems. However, the genus only accounts for a small percentage of all farmed mollusks. A much larger share of the produced mollusks globally belongs to Crassostrea spp. (including Magallana gigas) (FAO, 2018). Moreover, M. gigas and Ostrea edulis are both valuable products and have both proven possible to be grown successfully in an offshore setting (Pogoda et al., 2011) making a good case to be included in an offshore IMTA system.

Macroalgae The algae of an IMTA system is of crucial importance in the capability of the system to absorb dissolved nutrients. The ability of a species of algae of biofiltration is possible to quantify to estimate how large culture is needed to reach the aim of the farm, whether it is ecological or profitable. To estimate what algae species would be suitable for an IMTA farm, one should focus on the species’ potential of removing ammonium, phosphate, and nitrogen, as well as its optimal temperature range (Skriptsova and Miroshnikova, 2011). The seaweeds

growth in an IMTA system was limited by different factors at different times. By modeling the growth of algae in a newly set up finfish-sea urchin-seaweed system, Lamprianidou et al. (2015) found that the growth of the algae was in the first eight to ten months limited by nitrogen, this since the fish had not yet grown large enough to need much of feed and thus did not excrete nitrogen in excess yet. About eleven months after the system was started the limitation of the algae shifted from nitrogen to irradiation and to some extent also temperature, and the growth rate of the algae was high. To optimize the bioremediation capability of the algae, one should choose a location for the farm where irradiation and temperature are not the algae's limiting agents, but instead nutrients (Lamprianidou et al., 2015).

Different species of algae will contribute in different ways and to a different extent when grown in an IMTA system. Different species do also have different market values, which must be considered when choosing a candidate species.

Porphyra spp. has, for instance, proved to be a good candidate for IMTA farming, since the algae have thin blades and thus effectively absorb nutrients and providing a valuable product for the farmer to sell (Chopin et al., 1999). The product, Nori, is very valuable as a food with a market price of approximately US$ 66-166/kg sheet (Griffiths et al., 2016). However, Porphyra spp. does not have the same ability to store nutrients as other desirable macroalgae (e.g. kelp) but has a very high growth rate thus can be continuously harvested, removing the nutrients from the system (Chopin et al., 1999).

Laminaria japonica is a kelp with a steadily growing global production (FAO, 2018), and it can be refined to Wakame which is a valuable food product, valued at approximately US$ 50- 200/kg dried product (Griffiths et al., 2016). It is an important product in Northern China where it is grown together with oysters, abalone, and blue mussels (Troell et al., 2009) and thus could be a candidate for an IMTA system.

Another macroalgal candidate is Gracilaria spp. which can be used to make Agar, a highly valuable medicinal commodity and food, with an approximate value of US$ 5-100/kg as a powder. The Agar can also be further refined to agarose, also used in biotechnology, which in turn can sell for up to US$ 25000/kg (Griffiths et al., 2016). The production of Gracilaria spp. has increased severalfold in the last two decades, proving a large market (FAO, 2018). In a study by Bird, et al. (1982), Gracilaria spp. have shown a favorable attribute of “luxury“ uptake of nitrogen. The algae can store nitrogen when it does not require it for growth. In the study, Gracilaria spp. also showed an ability to more efficiently store ammonium than nitrate. Gracilaria spp. is thus an effective biofiltrator besides being of high marketable value and is thus a popular component of general aquaculture and IMTA. Gracilaria spp. has thus been the subject of many studies (e.g. Buschmann et al., 1994; Fletcher, 1995; Halling et al., 2005; Troell et al., 1997), several of which also reporting that the algae may be negatively affected by epiphytes reducing its growth rate and biomass.

A possibility for holothurians The most common idea of an IMTA is the finfish-bivalve-algae composition. However, several papers have proposed further optimization of the system by including holothurians and other echinoderms as detritus- and deposit feeders. holothurians, or sea cucumber, are a very valuable commodity especially in Asia, and goes under the trade name “Beche-de-Mer” when sold dried as food. The most expensive Beche-de-Mer in the Chinese market is the

Sandfish (Holothuria scabra) and Golden Sandfish (Holothuria lesson) selling for around USD 1668/kg in Hong Kong (Purcell, 2014). The value and their apparent ability to consume larger sedimented particles that otherwise falls lost have captured the interest of many IMTA developers and researchers (Cubillo et al., 2016; Nelson et al., 2012a; Neofitou et al., 2010, 2019; Paltzat et al., 2008).

An aquaculture farm does have an impact on the environment and ecological composition of life around, as well as beneath it, especially in oligotrophic systems such as the Mediterranean. Neofitou et al. (2010) found that there was a significant decrease in the number of species directly underneath a finfish aquaculture cage also with a higher abundance of individuals, in contrast to a control much farther from the cage, who experienced a higher and more even diversity index. This was credited to the additional food supply the farm provided, which attracted opportunistic species that came to dominate the benthic community (Neofitou et al., 2010). By using holothurians to feed on the settling particles that cannot be absorbed as efficiently by filter feeders such as mussels, the organic loading of the sediments can be decreased. Both the total nitrogen (Paltzat et al., 2008) and the total organic carbon concentration (Neofitou et al., 2019; Paltzat et al., 2008), as well as the total organic matter, (Neofitou et al., 2019) in the biodeposit, has shown to be lowered by the presence of holothurians. Thus, reducing the aquaculture emission of nutrients, which increases the overall performance of the farm and potentially allows for the farming to be practiced at a larger scale in oligotrophic environments such as the Mediterranean.

Although, with the environmental benefits in mind, the purely economic factors must be considered. holothurians generally must reach a certain size to be as profitable as possible for the market. Some, such as the Sandfish (H. scabra), Golden sandfish (H. lesson), Black teat fish (Holothuria whitmaei), and Herrmann´s sea cucumber (Stichopodidae hermanni) market value increases with size and thus pose to produce the largest specimens possible. Other species such as White teat fish (Holothuria fuscogilva) and Elephant trunkfish (Holothuria fuscopunctata) have a price optimum range where the specimens that have a ``medium´´ size sells for the highest price (Purcell, 2014). Due to these species-specific value optimums, one must assess when to harvest the holothurians for the best ecological effort and market price.

One stipulation of the inclusion of holothurians in an IMTA system is their ability to eat and process feed meant for finfish, in other words, feed that can be composed of terrestrial plants and/or artificial nutrients. In a long study of the Japanese common sea cucumber (Apostichopus japonicus), Yokoyama (2013) found that the holothurians grown underneath a fish cage grew larger than the control further from the cage. The author also compared specimens fed with artificial feed in lab with the ones grown underneath the fish cage in the field and noted a significantly higher growth rate of the individuals grown underneath the fish. Which allowed the author to conclude that the holothurians below the fish cage better could utilize the food available. The holothurians were thus shown to proliferate on a diet based on terrestrial ( C3 ) plants that the fish excretion and settling organic matter consisted of. The beneficial effects, for the holothurians, of integrated farming have also been reported in other studies. When modeling the output of a monoculture of the California sea cucumber (Parastichopus californicus) against several different compositions (all including the holothurians ) of IMTA, Cubillo, et al., (2016) found that an IMTA system consisting of finfish and holothurians promoted both the holothurians’ growth (i.e. its harvestable biomass) and its average physical appearance. However, it was also made apparent that the growth of the holothurians was not limited by the feed available. Instead, it was concluded that the temperature most probably was the limiting factor for holothurians growth. This since the

growth rate of the holothurian did not increase when increasing the density of fish Viz. the amount of food available. Cubillo et al., (2016) also found that a combination of oysters and holothurians help increase the holothurians’ growth by 40 %, a favorable effect that was also found by Paltzat et al., (2008). However, the latter author observed the issue of the seasonality of an integrated Pacific oyster (M. gigas) and P. californicus aquaculture, where in November only 25 % of the holothurians in the farm showed indications of feeding activity (i.e. growth). The density of the different components of the IMTA has also shown to cause effects, for instance, an increased density of holothurians resulted in a decrease of the average actual product of the holothurians but also in significant beneficial effects when concerning the emittance of effluents (Cubillo et al., 2016). This shall thus be premeditated with the absolute objective of the farm in mind, whether that is the economic or environmental sustainability.

Conclusions

The most important aspect of the development of an IMTA system is the composition of the cultivated species. When deciding which species that should be included one should first consider the sheer ecological and physiological ability of the concerned species to be able to proliferate in such a system. To evaluate and choose a candidate species (usually not applying to the intensive fed finfish) that is able to sustain itself on what is available in the system. After which the value of the species should be prioritized. The value is especially significant in an offshore setting where the investment and maintenance costs will be higher. Other aspects such as diversification, optimization, structural design, and further economic considerations are telling of the viability of an offshore IMTA system.

IMTA composition and diversification Diversification of the cultivated organisms in the same functional group would reduce the risk of an unexpected profit loss due to, e.g. a disease outbreak or a market value drop. It could also allow the farmer to have species with different harvesting seasons in the same functional group, thus allowing continuous biofiltration and a reduction of seasonal nutrient- and carbon- emission fluxes. For instance, cultivating Porphyra spp. or Gracilaria spp., and a Kelp such as L. japonica could result in a continuously high rate of nutrient removal. This, due to Porphyra spp. or Gracilaria spp. fast growth (Chopin et al., 1999), permitting more frequent harvesting. Furthermore, due to the Kelps’ longer growing time, and thus, slower harvesting frequency, the Kelp would provide a more stable and long-term nutrient sink. Both algae also providing profitable products (FAO, 2018). Gracilaria spp. trait of storing nitrate and ammonium especially effective is very favorable for biofiltration in an IMTA system. This since ammonium is the main byproduct of animal excretion (Bird et al., 1982). However, the trait is only favorable when considering its ability to reduce the effluent emission of the farm and not when considering the algae as a marketable product.

Another example could be the diversification with M. gigas and O. edulis, both providing a valuable product (FAO, 2018) and proliferate in an offshore environment (Pogoda et al., 2011). Since there is a disagreement in the literature over the actual contribution of bivalves towards reducing the particles originating from the aquaculture practices, one should focus on the ability of bivalves to reduce the nutrients on a regional scale in the area surrounding the farm rather than the local. Thus, primary viewing bivalves as an economic incentive and choosing the more valuable product that is oysters rather than Mytilus spp. One could also consider other suspension feeding-organisms that could fill the same niche as the bivalves in

an IMTA. One such is the Orange-footed sea cucumber (Cucumaria frondosa) which was found to be comparable in its biofiltration to the commonly farmed M. edulis (E. J. Nelson et al., 2012. a). However, C. frondosa´s overall marketability is unsure (E. J. Nelson et al., 2012. b). C. frondosa is thus not suitable as a cultivated species in an IMTA system. The pure marketable product that is bivalves is more appealing for cultivation.

Of potential deposit-feeding holothurians, the H. lessoni and H. scabra are the most valuable (Purcell, 2014). Although H. lessoni has the highest average price and thus was preferred for aquaculture by Purcell (2014) the most prominent holothurians occurring in studies of IMTA system are A. japonicus and P. californicus. Both have shown to effectively feed on finfish food pellets and finfish waste when simulated in computer modeling (Cubillo et al., 2016) or in experiments (Yokoyama, 2013). However, since A. japonicus has proven to be able to thrive when grown in coculture with finfish, it is preferable as a potential IMTA species.

Thus, a system consisting of a preferable finfish (e.g. S. salar) - Porphyra spp., Gracilaria spp., L. japonica - M. gigas, O. edulis – A. japonicus, P. californicus could be favorable. Different combinations of these to be possible to co-cultivate (e.g. Chopin et al., 1999; Cubillo et al., 2016; Paltzat et al., 2008; Pogoda et al., 2011; Troell et al., 1997; Yokoyama, 2013) and all proposed species in the chain has desirable attributes, subsequently, some combination could be a possible system for an IMTA system.

System optimization All optimization of the IMTA system does not have to result in a new aquaculture product. One type of optimization of the system could be to introduce Isopods or Amphipods to feed of epiphytes on the cultivated algae and the structure itself. This would not give the farm an additional product, nor would it directly aid the systems´ biofiltration capacity. However, it would increase the productivity of the cultivated algae. The reduction of epiphytes would be especially important when growing Gracilaria spp. which have proven to be heavily affected by epiphytic growth (Fletcher, 1995). A reduction of epiphytes would be favorable in offshore settings, particularly. For instance, epiphytic growth on Gracilaria spp. increase its drag through the water, thus making it more vulnerable to surge and storms. The fragility of Gracilaria spp. when affected by epiphytes could render it ill-fitting for aquaculture in a high energy offshore environment. However, since Gracilaria spp. is a very valuable species (Griffiths et al., 2016), the possibility of its co-cultivation with herbivores controlling epiphytic biomass should be considered. The fouling organism can have a great effect not only on the single cultivated organism but on the whole system as well (Sterling et al., 2016). Another possible optimization of the system could be the co-cultivation of herbivorous Echinoids. The co-cultivation of Strongylocentrotus droebachiensis and Mytilus spp. have shown a significant decrease in fouling on the structures of the IMTA (Sterling et al., 2016). Other Echinoids have also been able to sustain and proliferate on feces of holothurians (Sonnenholzner-Varas et al., 2019), and also been cultivated on feed consisting of macroalgae such as Ulva spp. (Shpigel et al., 2018), which also is a common epiphytic alga. If the inclusion of Echinoids would be possible, it would also produce a valuable product (Sonu, 1995), which is the Echinoid gonads.

Considering all statements above, a system of Finfish (e.g. S. salar) - Kelp (e.g. L. japonica), Gracilaria spp., Porphyra spp. – O. edulis, M. gigas – P. californicus, A. japonicus – S. droebachiensis, or comparable species. With a possible optimizing agent of Isopoda or Amphipoda could be a possible IMTA composition.

It is easy to strive for progressively more diversification and an increasing higher abundance of each cultivated species. However, this must stand in relation to, and will be limited by, the engineering possibilities of the farm structure, as well as the farm location´s features and limitations.

Site selection The selection of a site for the establishment of an IMTA farm is significant for the productivity and economy of the enterprise, as well as its environmental impact and disease control. For instance, as mentioned earlier, when considering bivalves, the selected location should be evaluated regarding the ambient particle concentration. A low concentration of ambient suspended particles should be sought after both when locating a site for the farm but also when managing the input of nutrients to the system, viz. feeding the finfish. Troell and Norberg (1998) found that pulse feeding of the fish may result in a particle concentration that would exceed the threshold for when bivalves´ start to produce pseudofeaces, subsequently, increasing the rate of sedimentation. The current and water circulation attributes of the site shall also be considered since it can benefit the productivity of the IMTA farm. Natural upwellings will allow the algae to enjoy nutrients as well as prolong the retention of particles in the water column, thus allowing for extended filtering of bivalves. Currents have also been attributed to the advantage of slowing the sedimentation rate (Troell and Norberg, 1998). Nevertheless, the cultivation of detritus feeders, such as holothurians, would reduce the issue of sedimentation overall and thus reduce the nutrient emission. Another aspect one must consider when choosing a site for the farm is the possibility to reduce the risk of a storm causing a resuspension event stirring up sedimented pathogens. This could be assured by locating the farm at a site with a water column depth of more than 50 meters (Wiberg, 2000).

Structural design The Offshore ring-design proposed (and patented pending) by Buck and Buchholz (2004) is a promising structural system for offshore macroalgae aquaculture. The main advantage of the system was the ability to let the algae grow and attach themselves to the ring structure inshore before towing the structure out to the offshore site. Thus, reducing the risk of waves damaging and/or knocking of the cultured organism. In the study, the authors proposed the system as a possibility for the future development of integrated aquaculture. An IMTA system could be developed around a Ring-design macroalgae structure. The algae should be grown at least at a depth of one to one and a half meters to protect it from harmful UV and turbulence of the upper surface layer (Buck and Buchholz, 2004). However some algae, such as Porphyra spp. can, if wanted, be grown even deeper at 10 - 40 m depth (Chopin et al., 1999). Nevertheless, the ring system is possible to modify to the preferred depth. Potential bivalves should be located in the intercept of falling particles from the finfish cage to be effective according to Cheshuk et al (2003). That is within 50 meters from the finfish cage and at least 5 meters deeper. Consequently, the amount of area suitable to bivalves would be limited and directly linked to the size of the fish cage. Meaning, a larger fish cage gives a larger circumference of suitable bivalve area. Additionally, this allows for the cultivation of algae either above the bivalves or further away than 50 meters from the fish cage. However, this would require a ring structure for the algae that would be of much larger diameter than the 5 meters diameter proposed by Buck and Buchholz (2004). In a high energy offshore setting, structural integrity is of the essence and thus must be prioritized. Several smaller rings around the fish cage and above the bivalves could allow the cultivation of more

algae without compromising the structural integrity of the ring design. However, the restriction of the individual ring size as of today may indicate that the placement of more and less vulnerable species must be carefully considered. For instance, if an IMTA farm would cultivate Kelp and the more fragile Gracilaria spp a more central placement of the Gracillaria might be more favorable. This both since the Gracilaria spp. is more fragile, but also since it is more effective at absorbing ammonium released from the finfish in the center of the farm. Thus, both protecting the Gracilaria spp. and allowing it to more efficiently absorb nutrients. In the case of holothurians, Yokoyama (2013) showed a successful cultivation technique of A. japonicus by suspending them beneath the finfish cages. Thus, allowing the offshore IMTA cultivation of holothurians at deeper sites. The design of the system seems to be crucial for its success (Chopin pers comm)

Economics A prominent problem of IMTA and the diversification of the system is that it will cause the system to become increasingly complex, thus risk alienating potential aquaculture farmers considering the adoption of an IMTA system. Especially when considering the already elevated costs of offshore investment. Although, the large initial investment could also render the farmer to be more concerned with the sustainability of the income and thus welcome a diversification and the economic stability it can contribute. The most probable cause will be that developers with a large capital will be the most likely to establish an offshore IMTA farm and cooperate with other industries in an effort to cut costs and exercise larger sway over policymakers. The industries best suited for cooperation with offshore aquaculture seems to be energy industries, especially offshore windmills.

Summary Integrated multi-trophic aquaculture is a complex system to operate and develop, and to bring it offshore makes it even more difficult. This results in the exceeding importance of preparations and the deliberate and conscious consideration of all factors involved. That includes the site of the farm, the species to cultivate, and the potential of cooperation with other industries. In the present study, an orientation of the main concerns of an offshore IMTA farm were presented and the possibility to optimize the system was evaluated. An offshore establishment of IMTA will require extensive site assessments but is viable. The ring design proposed by Buck and Buchholz (2004) is a possible design for the structure of the farm. However, the design of the structure must be possible to scale up and still hold its structural integrity to accommodate a more complex IMTA system. Optimization of future offshore IMTA farms could occur by including holothurians in suspended platforms.

To further investigate the viability of offshore IMTA, more research needs to be done of the structure itself and how an upscaling could ensue. Also, when optimizing the system by the addition of holothurians there is a need to further study how the holothurians would be affected by feeding on the sedimented particles from the farm, in reference to the pathogen buildup recognized in the pseudofeaces of bivalves. Acknowledgment:

I would like to thank Michael Tedengren for taking his time to give valuable feedback and to guide me through the writing of this article. I would also like to thank, Matilda Granberg, Benjamin Norgren, and Alexander Stockhaus for their input.

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