Low trophic species in aquaculture—growth and research challenges

The past 50 years of growth in global aquaculture have helped address pressing human dietary protein needs. Any further increase in aquaculture production must be made without compromise to the future environmental well-being of aquatic environments and the organisms, including human beings, dependent on those environments. This essential continuation of growth cannot be sustained with increased production of high trophic level species alone, despite their intrinsic high economic value and the contribution they make to world food supplies. The production of aquaculture species, which feed at low trophic levels, exhibits convincing potential to support large-scale increases in production volumes while, if appropriately applied and managed, avoiding environmental impacts. For the purposes of this article, we have defined low trophic species as primary producers and primary consumers. In an aquaculture context, we have included species consuming detritus. There is ongoing discussion regarding the trophic levels of fed species that are higher trophic levels than primary consumers (Cottrell et al., 2021). These are commonly referred to as "fed" species and research has shown that the trophic levels of a number of "fed" aquaculture species has reduced significantly over the past decades as a result of changes to manufactured feeds and the increasing inclusion of land-based proteins to replace marine proteins. However, here we focus primarily on "extractive" and herbivorous, low trophic species. From a marine perspective, examples of primary producers are micro-and macroalgae, while herbivorous fish and invertebrates are primary consumers. These definitions are not completely accurate, particularly in the case of herbivory, with many filtering species consuming a variety of phytoplankton and zooplankton. Equally, detritivores consume a wide variety of infauna and herbivorous aquaculture species are often fed formulated diets enriched with animal by-products. In the interest of simplicity, these partial inclusions of animal diet will be disregarded in the following text, apart from the noteworthy need to reduce or remove animal by-products inclusion from aquaculture diets for herbivorous species. Low trophic species already dominate global aquaculture in terms of production volumes. Currently, key primary producers in aquaculture are led by the main macroalgae species produced Sacharina japonica along with Eucheuma spp. making up more than 50% of global production. With worldwide algae production of 35 million tons per annum, the sector is second only to freshwater finfish in global output from aquaculture (FAO, 2022). Small but economically important contributions and primary production output in aquaculture are made by microalgae often used in dietary supplementation for humans and animals and the production of valuable nutraceuticals, pigments, and other high-value extracts. Mollusks, overwhelmingly bivalves (which are primary consumers), make up the third most important overall production sector in global aquaculture with 18 million tons per annum. The vast majority of the 45 million tons of freshwater finfish produced globally are also considered primary consumers; however, as mentioned above, an increasing amount of fishmeal input to diets is reducing the herbivorous nature of this form of aquaculture. The production of low trophic aquaculture species benefits, in terms of sustainability, from the significant reduction in feed energy input requirements, based on the usual assumptions of energy loss when moving up trophic levels. This translates into reduced energy inputs into formulated feeds for herbivorous species, zero input for primary producers and extractive or unfed species such as bivalves, sponges, and detritivores such as sea cucumbers. In addition, primary producers and shellfish have the potential to create genuine environmental benefits in terms of uptake of excess carbon dioxide and nutrients in the marine environment (Park et al., 2021). Overall, the arguments for expansion of aquaculture production globally, through low trophic species production, are overwhelming in terms of scalability, level of sustainability, and potential for future sequestration and mitigation in the Anthropocene. It is extremely encouraging to see large international funding/research bodies clearly defining the need for research and development of low trophic species and unfed aquaculture, for example, "European Commission strategic Guidelines for aquaculture" 2021: "Promoting the development of … aquaculture systems with lower environmental impact … diversification to lower-trophic species (mollusks and other invertebrates and algae and herbivore fish)" (EC, 2021). There are a number of research focuses that have been identified by scientists and funding bodies globally to further the growth of low trophic species aquaculture. The first area of research that we wish to highlight is the rapid development, commercialization, and upscaling of production facilities for extractive species at very significant scales. This includes kilo-hectare scale production of established species of macroalgae and mussels using established longline production methods. This must be expanded upon and made more sustainable with improved alternative large-scale production methods. Limitations on nearshore space access require the successful implementation of improved engineering to allow such structures in available offshore locations. In addition to engineering, site selection methods must be further optimized and applied to ensure operability, suitability of the species, and availability of nutrients/feed sources. Longer term increases in this form of production can be achieved through the development of novel species equally suited to production in very large-scale offshore open aquaculture systems such as long lines. The establishment of production methods for novel low trophic species, in particular, extractive species or detritivores, is also extremely desirable. Specific examples here include high-value macroalgae species, high-value mollusks, and detritivores. While detritivore species may not scale up as rapidly, they may offer higher value end-products easily integrated into established value chains. The development of other novel species for low trophic aquaculture in freshwater is also desirable but must take into account increasingly limited freshwater resource availability and the requirement to ensure low water use along with high protein and economic yields. Market demand for the products arising from low trophic species aquaculture will be central to the overall success of all the above initiatives and long-term establishment of production at scale. Some species are well established and of high economic value, such as oysters, pearl mussels, Caulerpa lentillifera, and bighead carp. Unfortunately, many other low trophic species in aquaculture are considered medium-to-low value, some are too bony or have flavor profiles that do not fit into culinary habits of consumers in local markets, and many other species and development are niche products or their value is unknown in traditional markets. The key to creating market demand on a scale that would support large-scale production of many low trophic species will be developing products that meet the specific consumer taste, texture, and product form preferences in the markets to be targeted. In addition to the provision of valuable protein and other nutrients, low trophic species must be developed as contributing other resources for human use. If large-scale macroalgae culture for sequestration of anthropogenic carbon emissions is to be established, there must be market demand, supported by appropriate regulatory frameworks to allow emission offsets, although algae production is essential. Adding value to low trophic species' aquaculture outputs through technical innovation is key to establishing their use as additional resources. Technical innovation in terms of processing, extraction, and biorefining of abundant low trophic aquaculture biomass will allow novel value chains to develop and enhance economic viability of sustainable production. Technologies to reduce muscle bone load and develop prepared or high trophic species replacement products from low trophic species readily produced and consumed in Asia may enhance demand among Western consumers. Equally technical innovation to produce low trophic aquaculture species in conjunction with other industries and "fed" aquaculture in such a way that the low trophic species act as nutrient sinks, system cleaners, or biological filters providing essential services while improving sustainability of aquaculture areas and producing additional product (Onomu et al., 2023). However, integrated production systems are difficult to manage. Part of the management challenge is that it is not possible to optimize production at the lowest cost per kg of production for all crops integrated into one production system (Neori et al., 2017). Thus, not all crops will be produced at the lowest cost level and those not optimized will be less competitive and potentially not viable in the market. As with all aquaculture development, regulatory and legislative structures require improvement to allow access to aquatic resources and space for aquaculture operators to exist and grow. It is important to note and praise the increased apparent willingness of governments worldwide to provide access in the marine environment for such developments. Nonetheless, further development of optimal legislature to enable and protect aquaculture production in onshore and offshore environments is essential. A cautionary note should be taken from terrestrial culture methods in terms of altering environments to support the growth of primary producers and primary consumers. It is imperative that legislative environments are balanced and protective too, ensuring that aquaculture o

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