4.1. Different type of waste, different scales for mitigation

Effective mitigation strategies against potential environmental drawbacks derived from aquaculture waste must follow an ecosystem-based approach taking into account suitable spatial scales according to the area of dispersion of this waste (Costa-Pierce and Page, 2013). Since particulate and dissolved waste have markedly different dispersion dynamics (Tett, 2008; Sanz-Lázaro et al., 2011; Jansen et al., 2018), adaptive scales should be considered depending on the type of waste.

In the case of particulate waste, bioremediation strategies should focus on the farm scale because their sedimentation mostly occurs in the first hundreds of meters from the aquaculture facility (Holmer et al., 2007; Sanz-Lázaro et al., 2011). Furthermore, suitable low trophic level candidates that are able to consume a substantial part of the particulate waste must be selected. Deposit feeders, such as sea cucumber, are good candidates, since they feed on the benthic system where particulate waste has a much higher persistence than in the water column (Cubillo et al., 2016). Thus, in this case, it is suitable to locate high and low trophic level cultures in close vicinity.

Dissolved waste is rapidly dispersed by currents. Thus, cultures that can sequester nutrients (macroalgae) or limit the derived primary production (bivalve molluscs), do not necessarily need to be in the close vicinity of the fish farms. These cultures need to be located in the area along which most of these nutrients or the derived primary production are dispersed, which is generally the water body area.

4.2. IMTA artificial boundaries: an enclosed concept used in open systems

IMTA concept of low trophic level cultures using the waste generated by high trophic level cultures justifies the location of both types of cultures in the close vicinity in closed systems, such as in terrestrial aquaculture ponds, or in very enclosed coastal areas. But locating low trophic level cultures in close vicinity to high trophic level cultures, aiming to sequester dissolved waste in an open system, is comparable to planting trees close to factories that emit CO₂, aiming to reduce their carbon footprint.

The apparently restricted feasibility of IMTA using bivalves and macroalgae in the water column is constrained by its implementation linked to the farm scale. The persistence of dissolved waste in fish farm leases located in open areas is so limited, that the ability of the low trophic cultures to assimilate them or the derived primary production is scarce. Thus, IMTA should be managed in terms of ecosystemic functionalities rather than absolute distances considering the scale of the reach of the waste (Chopin, 2013; Sanz-Lazaro and Sanchez-Jerez, 2017). In the case of dissolved waste, cultured macroalgae and bivalve molluscs can do their job even when these species are not in the close vicinity of the facility, as long as they are located within their area of dispersion.

4.3. RIMTA: Spatially separated, ecologically linked

Despite the above-mentioned recommendations, the localized concept of IMTA for dissolved waste has not been revised, and its implementation to industrial-scale keeps on being hindered by its own artificial boundaries, always culturing the species of low trophic level in close proximity to high trophic level species. IMTA should focus on the scale at which low trophic level species are able to sequester the waste generated by fish farming, which in the case of dissolved waste corresponds to the water body where it is located. Considering the spatial scales defined in ECASA toolbox (https://cordis.europa.eu/project/id/6540/reporting), typically IMTA has focused on zone A (local, farm-scale). However, IMTA using macroalgae and bivalve molluscs should move to zone B (small water body scale) and C (regional scale). The management of fish farms located in highly enclosed water bodies such as lakes, coastal lagoons, fjords and lochs, should be done at the scale of zone B; while off-coast and offshore farming should be done at the scale of zone C (Fig. 2).

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Fig. 2. Spatial scales of integrated multitrophic aquaculture (IMTA) and regional integrated multitrophic aquaculture (RIMTA).

We propose the concept of Regional Integrated Multitrophic Aquaculture (RIMTA) that is defined as the culture of low trophic level species such as macroalgae and bivalve molluscs, to mitigate the ecological negative effects derived from the input of dissolved nutrients from fed aquaculture. RIMTA is an ecosystem-based approach that takes into account the ecological processes, human-induced pressures and their respective spatial scales. Accordingly, RIMTA acknowledges that low trophic level species do not necessarily need to be placed in the close vicinity of the fish farm as long as it is located within the area of dispersion of the fish farm waste (Fig. 3).

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Fig. 3. Scheme comparing integrated multitrophic aquaculture (IMTA) and regional integrated multitrophic aquaculture (RIMTA) rationales. POM stands for particulate organic matter. Arrows indicate fluxes of matter.

Defining the scale and the boundary of a water body must be done carefully to assure that aquaculture leases, despite being spatially separated, they are communicated. Since this may not always be straight forward, in many cases, tracer studies or Lagrangian ocean analysis (van Sebille et al., 2018) should be required for a suitable site selection of macroalgae and bivalve culture leases. Examples of fish farm dissolved waste transport are already available (Venayagamoorthy et al., 2011).

RIMTA also acknowledges that the high dispersion of dissolved waste lowers the capacity of the low trophic level cultures to specifically feed on nutrients or the derived primary production released by high trophic level cultures. Additionally, nutrient input is a global anthropogenic driver of ecological change and several anthropogenic activities release nutrients to the environment (Halpern et al., 2008). Thus, irrespectively of the origin of the nutrients (from high trophic level aquaculture or from another anthropic source) that the low trophic cultures sequester, the low trophic culture will reduce the regional nutrient input or the derived primary production to which high trophic level aquaculture is contributing.

4.4. Implementation benefits of RIMTA

The balance of trade-offs between the benefits and costs of adopting IMTA is currently not sufficiently positive to motivate the IMTA implementation in Europe (Hughes and Black, 2016). This is partly due to the problems derived from culturing potential fouling species in close vicinity to fish farms, which can pose risks related to the increase of the biofouling in fish farm nets, reducing the water exchange and compromising fish health. RIMTA also facilitates the establishment of aquaculture facilities from a legal perspective. For example, in Europe, administrative processes and decisions dealing with aquaculture lease concessions are generally slow, especially for fish farms culturing different species (Hedley and Huntington, 2009). Monocultures have easier lease regulations in terms of bureaucracy and requirements which can speed up these administrative processes.

Separating both types of cultures will promote low trophic level aquaculture. This will not only foster the sustainability of low trophic level species, but of aquaculture in general. First, macroalgae and bivalve mollusc aquaculture do not need to be fed, releasing pressure to fish or other food stocks. Second, this type of farming facilitates local entrepreneurship, since the investment needed is low compared to other types of aquaculture. Third, macroalgae and bivalve molluscs are valuable food, being a source of protein- and omega-3, which can be directly used for human consumption or, indirectly, incorporated in formulated feeds for fish and other farmed species (Tiwari and Troy, 2015; Carboni et al., 2019). Consequently, low trophic level aquaculture can release pressure from agriculture and fisheries, activities with a stagnant production (DG RTD European Commission, 2017), and promote the farming industry.

4.5. Ecological interactions of RIMTA

The enhancement of macroalgae and bivalve mollusc aquaculture, apart from nutrient sequestration, can favour another key ecosystem service, such as climate change mitigation, through their use as biofuels (Hossain et al., 2008) or by acting as carbon sinks (Hill et al., 2015; Xiao et al., 2017). However, we need to keep in mind that the intensive cultivation of macroalgae and bivalves can lead to some negative ecological consequences.

The structures for culturing macroalgae and bivalve molluscs slow down currents, increasing the residence time of the water and sedimentation which may cause habitat modifications in the pelagic and benthic system (Buschmann et al., 2008). As regards bivalves, they need to be cultivated on appropriate densities, depending on the oceanographic conditions such as depth or current intensity to avoid environmental drawbacks in the benthos due to the release of particulate waste (Dumbauld et al., 2009; Fabi et al., 2009). Additionally, extensive bivalve cultures can lead to the depletion of planktonic organisms (Hulot et al., 2018). Thus, oceanographic variables related to potential benthic environmental drawbacks, such as current intensity or depth, as well as carrying capacities, should be taken into account in the location where the culture will be deployed (McKindsey, 2012). Caution should be taken in shallow, enclosed, eutrophic and low energy areas such as the Baltic since experts do not reach consensus on the suitability of bivalve aquaculture due to possible increased nitrogen benthic fluxes derived from organic deposition through pseudo-faeces (Cranford et al., 2007; Stadmark and Conley, 2011).

4.6. RIMTA sustainability

RIMTA, following an ecosystem-based approach, searches for sustainability integrating stakeholders in an equitable way. The full development of RIMTA must be associated with the recognition of the above-mentioned valuable ecosystem services, mainly nutrient and derived primary production sequestration, that macroalgae and bivalve mollusc cultures provide. Since these types of cultures can have a low monetary return compared to fed cultures, RIMTA should be accompanied by tax benefits for farmers that implement it or from nutrient trading schemes, which have already been proposed for reducing eutrophication in the Gulf of Mexico (Perez et al., 2013) or the Baltic Sea (Lindahl and Kollberg, 2009). Taxes on marine pollution (ecotaxes) provide incentives to polluters to reduce emissions and seek out cleaner and sustainable alternatives (Davis and Gartside, 2001). In our case, these ecotaxes would promote the sustainable use of natural resources, providing economical advantages to fish farm companies that lease low trophic cultures within the water body affected by fish farming. Thus, aquaculture companies will reduce the nutrient footprint or even become nutrient neutral, and indirectly, will lead to aquaculture diversification favouring the development of IMTA. Additionally, the nutrient sequestration produced by RIMTA would contribute to achieve a good environmental status in marine water bodies (Marine Strategy Framework Directive, 2008/56/EC). The independent allocation of high and low trophic level cultures, followed by economical support, which should be explicitly supported by corresponding administrations through laws and regulations, is needed to ensure the implementation of RIMTA and its sustainability.