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The Underexplored Potential of Green Macroalgae in Aquaculture

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The Underexplored Potential of Green Macroalgae in Aquaculture Received: 15 October 2020 | Revised: 3 April 2021 | Accepted: 10 May 2021 DOI: 10.1111/raq.12580 REVIEW The underexplored potential of green macroalgae in aquaculture Anthony Moreira | Sónia Cruz | Rúben Marques | Paulo Cartaxana Centre for Environmental and Marine Studies (CESAM) & Department of Abstract Biology, University of Aveiro, Portugal Green macroalgae (Chlorophyta) currently represent a residual fraction (<1%) of Correspondence global seaweed biomass production landings. In turn, red (Rhodophyta) and brown Paulo Cartaxana, Department of Biology, University of Aveiro, Campus Universitário (Ochrophyta) macroalgae dominate the remaining percentage of aquaculture produc- de Santiago, 3810- 193 Aveiro, Portugal. tion, exceeding 32 million tonnes per annum. However, the industry relies on a rela- Email: [email protected] tively low number of species, in which as few as seven macroalgal genera collectively Funding information represent the bulk of global production metrics. At present, innovation and increased Fundação para a Ciência e a Tecnologia, Grant/Award Number: sustainability of the industry calls for diversification of macroalgal species/strains in CEECIND/01434/2018, PTDC/ aquaculture to counteract potential adverse effects ensuing from genetic impoverish- BIA- FBT/30979/2017 and UIDP/50017/2020+UIDB/50017/2020; ment, decreased resilience to disease and climate change. Despite the dominance of European Regional Development Fund, red and brown seaweed regarding production figures, aquaculture of green macroal- Grant/Award Number: PTDC/BIA- FBT/30979/2017 gae has witnessed an increasing trend in productivity and diversification over the last decades, particularly in Asia, where green seaweed taxa often occupy specific market niches in the food sector. Furthermore, growing interest in green seaweeds in aquaculture has been highlighted for different applications in emerging western markets (eg IMTA, biorefineries, food delicacies), owing to a unique diversity of cy- tomorphologies, ecophysiological traits, propagation capacities and bioactive com- pounds featured by this group of macroalgae. Cultivation technologies are relatively well developed, but sustainability assessments are scarce and required to unlock the potential of green seaweeds. Although it is likely that green macroalgae will remain occupying specialised market niches, in which high- value products are favoured, we argue that aquaculture of chlorophytan taxa presents itself as a compelling option under the current quest for commercial diversification of products and expansion of the sector. KEYWORDS bioactive compounds, cultivation techniques, integrated multitrophic aquaculture, life- cycle assessment, seaweeds, Ulvophyceae All named authors contributed significantly to this work and agree with the content of the manuscript. Financial support is fully acknowledged, and the authors declare no conflict of interest. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2021 The Authors. Reviews in Aquaculture published by John Wiley & Sons Australia, Ltd Rev Aquac. 2021;00:1–22. wileyonlinelibrary.com/journal/raq | 1 2 | MOREIRA ET AL. 1 | INTRODUCTION traction given the increasing perception of algae as healthy and sus- tainable foodstuffs, particularly in developing markets of western Macroalgae (or seaweeds) comprise a diverse group of photo- cultures.2 1 – 2 3 synthetic, multicellular, eukaryotic organisms assigned to either The bulk of macroalgae aquaculture takes place in South- the Plantae or Chromista kingdoms. Most are marine, where they East Asian and Pacific countries, of which China, the Philippines, play predominant roles as primary producers in coastal waters of Indonesia, Republic of Korea and Japan contribute a staggering the planet.1 Despite being avascular and lacking true roots, stems, ~98% of global seaweed biomass production, while the same indus- leaves and complex reproductive structures, some macroalgae dis- try is sustained by as few as seven macroalgal genera, all of which play plant- like appearances, in that they present differentiated thalli assigned to either Rhodophyta or Ochrophyta.19 Some of these mac- with attachment organs (holdfasts), stem- like structures (stipes) roalgae are destined for the hydrocolloid industry, such as Eucheuma and photosynthetic blades (fronds).2 Marine macroalgae can be di- spp., Kappaphycus alvarezii and Gracilaria spp., whereas other taxa vided into three phyla: Chlorophyta (green), Rhodophyta (red) and are used directly as human food, namely Saccharina japonica, Undaria Ochrophyta (brown), classified according to photosynthetic pigment pinnatifida, Sargassum fusiform and Pyropia spp.19,24 In turn, the out- content, carbohydrate reserves, cell wall components and flagella put of green macroalgae (Chlorophyta) aquaculture currently rep- construction and orientation.1 Collectively, the diversity of these resents only a fraction of global landings (<1%), lagging well behind groups exceeds 10,000 species, while new taxa are described every the most relevant taxa in terms of production metrics. Despite pre- year. Currently, more than 1500 macroalgal species are assigned senting comparably lower production figures, the aquaculture of to Chlorophyta; approx. 2000 to Ochrophyta; and about 7300 to green seaweeds has witnessed an increasing trend in productivity Rhodophyta.3 Together, macroalgae constitute an important biolog- and commercial diversification over the last decades (Figure 1).19 ical resource, providing a variety of ecosystem services and socio- Nevertheless, asymmetries deriving from the dominance of few taxa economic value.4,5 in macroalgal aquaculture intensify the need for increased innova- Since prehistoric times, ca. 160 thousand years ago, early homi- tion and sustainability of the industry. Particularly, the commoditisa- nids have relied on intertidal habitats as foraging grounds for marine tion of the industry is thought to be inconsistent with future demand resources.6,7 Eventually, the inclusion of macroalgae in human diet of high- value seaweed products, by failing to provide standardised, is thought to have prompted profound impacts upon the evolution high quality, traceable products.25 Advances are therefore required of human civilisation.8,9 The earliest evidence of the relationship to meet the challenges of an evolving industry, through species between humans and marine macroalgae dates to the Neolithic and/or cultivar diversification, standardisation of cultivation tech- (ca. 14,000 years ago) according to archaeological findings, when niques and increased awareness of local genetic and environmental humans seemingly collected and transported a variety of seaweed variability.18,20,25,26 species to be used as foodstuffs, trade items and ancient pharmaco- In this context, expanding green macroalgae aquaculture peia.10 In addition, written records support that seaweed harvesting emerges as a compelling solution towards the diversification and has been going on for centuries in virtually all shoreline areas where improvement of the sector, by providing a diverse pool of largely coastal communities have established, namely in Asia,11 Europe,12 untapped biological resources, with intrinsic potential to unlock an Americas,10 Oceania13,14 and Africa.15 Such communities relied on array of different biotechnological applications. Indeed, due to the marine macroalgae for a variety of different purposes including evolutionary divergence between the major macroalgae phyla, the human and animal feed, soil fertilisation, medicinal, cultural activi- Chlorophyta, Rhodophyta and Ochrophyta differ in their elemental ties and raw material for different applications.14,16 composition,27 metabolomic28,29 and fatty acid profiles,3 0 – 3 3 nutri- Like other organisms included in human diet and well- being, some tional properties,34,35 polysaccharide types36 and organoleptic prop- macroalgal species were domesticated and cultivated, once growing erties.37 Ultimately, distinctive features among macroalgal phyla will demand exceeded natural beds’ holding capacities.17,18 Modern cul- allow different applications, and therefore innovation in the indus- tivation technologies first emerged in the 20th century in China and try. Accordingly, green macroalgae have been recently promoted in Japan, after the description of the reproductive cycle of bladed for different applications, including biorefinery operations,38 land- Bangiales (Pyropia sp., Rhodophyta).11 Soon after, the aquaculture based integrated multitrophic aquaculture (IMTA) systems39,40 and of macroalgae rapidly expanded into what currently represents ap- high- value food products in modern cuisine.41 Examples of devel- proximately half of global marine aquaculture production landings oping industrial applications using green macroalgae as raw material (51%), comparing to molluscs (27%), fish (13%) and crustaceans (9%); include the extraction of cellulose42 or sulphated polysaccharides43 while exploitation of natural stocks represents a fraction (~2.8%) of and the production of biochar,44 bioethanol45 and bioplastics,46 total production of seaweeds.19 Macroalgal production is nowadays while an indefinite number of bioactive molecules will keep emerg- the fastest growing sector in global marine aquaculture generating ing from green macroalgae metabolite screening studies.47,48 an excess of US$
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