REVIEWS

Bivalve Mariculture in Two – Way Interaction with Phytoplankton: A Review of Feeding Mechanism and Nutrient Recycling

1 2 3 Rasheed1Department Olatunji of Fisheries MORUF and*, Gabriel Aquaculture, Femi OKUNADE Bayero University,, Owoyemi Kano, Wahab Kano ELEGBELEYE State, Nigeria 2Department of Biological Sciences, Yaba College of Technology, Lagos State, Nigeria 3Department of Marine Sciences, University of Lagos, Akoka, Lagos State, Nigeria *corresponding author: [email protected]

Bulletin UASVM Animal Science and Biotechnologies 77(2)/2020 ISSN-L 1843-5262; Print ISSN 1843-5262; Electronic ISSN 1843-536X DOI:10.15835/buasvmcn-asb: 2020.0010

Abstract

Bivalve mariculture is a type of molluscan farming done in open seawater on racks, rafts or longlines where naturally occurring phytoplankton serves as a key food item, introduced into the enclosures with the normal circulation of seawater. Increasingly, the reverse trophic interaction is being recognized; dissolved inorganic and organic waste compounds released by metabolically active bivalves can supply phytoplankton with nutrient and energy requirements for their growth. This two-way interaction can be viewed as a type of community symbiosis developed over long evolutionary timescales. The extent to which this affects overall nutrient budgets and thus primary production is related to the system flushing rate and residence time. Here we reviewed the feeding mechanism and nutrient recycling activities of bivalve and also emphasized the role of phytoplankton as a key nutritional live feed in sustainable bivalve mariculture. Bivalves influence nutrient dynamics through direct excretion and indirectly through microbial mediated remineralisation of their organic deposits in the sediments. The quantitative knowledge of bivalve - phytoplankton trophic interactions in coastal waters will inform bivalve maricultureKeywords: development to effectively, serve the needs of both seafood production and ecosystem restoration.

bottom-feeder food web, microalgae, mollusc farming, symbiosis.

Introduction

in coastal and offshore waters where salinity is Mollusks are important resources that maximal and not subject to significant daily or contribute considerable economic value to the seasonal variation. Mariculture has more recently world’s fisheries. The global production of marine become an important source of bivalve, which is mollusk for human consumption is more than 17 the focus of this review. million tonnes in the year 2018, with China as the Bivalves as a group have noet al head and they major producer with relatively highest percentage lack some usual molluscan organs like the radula of production (FAO, 2020). In terms of mariculture and the odontophore (Romano ., 2014). They (disregarding freshwater production), mollusc include the clams, oysters, cockles, mussels, production exceeds finfish production value by scallops, and numerous other families that live underover 900-fold controlled (Mau or &semi Jha, 2018).controlled As acondition concept, in saltwater, as well as a number of families that mariculture is the rearing of aquatic organisms live in freshwater. Bivalve mariculture is a type of molluscan farming done in open seawater 2 and al.

MORUF on racks, rafts or longlines. The commercial fast rate of primary production (Gao & Campbell, importance of bivalve mariculture include but 2014). Phytoplankton are the autotrophic (self- not limited to food security, pearl production feeding) components of the plankton community Crassostreaand lime manufacture. madrasensis, As C. gryphoides,listed by Narasimham C. rivularis and a key part of oceans, seas and freshwater ba- and(2005), Saccostrea popular cucullata culture species of oysters include sin ecosystems. According to Pal and Choudhury are Perna viridis and P. indica (2014), phytoplankton are free-floating photo- clams are Villorita cyprinoids,; culture Paphia species malabarica, of mussel synthetic aquatic microorganisms, which move Meritrix casta and Anadara; culture granosa species of from one place to another, either actively by their Chlamys barrei, C. locomotor organs (flagella) or passively by water nobills, Placopecten magellanicus and Argopecten while currents. Today, the contribution of phytoplankton irradians.culture species of scallops are to the biosphere continues to be unique because this group largely contributes to the renewal of the atmospheric oxygen and acts as a tremendous 2 One of the factors that influence bivalve etsink al for CO , which is used for the synthesis of or- growth in both natural populations and maricul- ganic compounds through photosynthesis (Nelson ture conditions is availability and quality of food. ., 1995). While accounting for less than 1% of Traditionally, phytoplankton was considered as Earth’s biomass, et al. phytoplankton is responsible for primary food source for bivalves (Gosling, 2003). more than 50% annual net biomass production However, a number of studies pointed out that en- (Bowler , 2010). ergy is also derived from other food sources such Phytoplankton differentiate from other plan­ as bacteria, detritus and even zooplankton (Le- ktonic taxa by the presence of photosynthetic hane & Davenport, 2006). Through filter feeding, mem­branes. This makes them produce biomass bivalves play important role in marine ecosystems by autotrophically converting naturally occurring by controlling abundances of primary producers, carbon into protoplasm. In this way, phytoplankton zooplankton and larval stages of other marine function as the foundation of the marine food web species. By this process, bivalves haveet al. great influ- by supporting all other life in the ocean. Food webs ence in energy and nutrient flux between benthic are built from food chains. All forms of life in the and pelagic communities (Arapov , 2010). sea have the potential to become food for another The two-way interaction between bivalve life form. In the ocean, a food chain typically starts mariculture and phytoplankton fundamentally with energy from the sun powering phytoplankton, involve feeding and nutrient recycling activities and follows a course shown in Figure 1. of bivalve molluscs, which tend to sustain primary Phytoplankton community supports the base production locally. This paper aimed to give an of the natural food chain depending on which overview of current understanding on bivalve’s the natural fauna including the fish populations feeding mechanism and to emphasize the role can survive (Napiórkowska-Krzebietke, 2017). A of phytoplankton as a key nutritional live feed in simplified classical food web in an aquatic ecosys­ bivalve mariculture, by reviewing the worldwide tem comprises phytoplankton as staple food for literature through Internet search engines, zooplankton, and further zooplankton as food textbooks and theses. Literatures obtained were for planktivorous fish, which in turn are food analyzedPhytoplankton in pros and as a relevant Basic Element cited figure in a and for predatory fish. A 2017 study estimated the headingsClassical were Food adopted. Web nutritional value of natural phytoplankton in terms of carbohydrate, protein and lipid across the world ocean using ocean-colour data from satellites, and Unlike terrestrial environments, marine en- found the calorific value of phytoplankton to vary vironments have biomass pyramids which are considerablyBiologically across Active different Ingredients oceanic of regions and inverted at the base. In particular, the biomasset al. of betweenPhytoplankton different times of the year (Roy, 2018). consumers (copepods, krill, bivalve) is larger than the biomass of primary producers (Arapov , 2010). This happens because the ocean’s primary Phytoplankton produce valuable compounds producers are tiny phytoplankton, which grow that include crucial phytonutrients and biological- Bulletinand reproduce UASVM Animal Sciencerapidly, and Biotechnologiesso a small 77(2)mass / 2020 can have a ly active ingredients, e.g. fatty acids, amino acids, 3

Bivalve Mariculture in Two – Way Interaction with Phytoplankton: A Review of Feeding Mechanism and Nutrient Recycling

Figure 1.

Summary of phytoplankton as a basic element in a classical food web

Figure 2.

Notable biomolecules from phytoplankton biomass carotenoids, chlorophyll, vitamins, antioxidants 2013). These bio-compounds play physiological (Figure 2). Thus, thorough nutritional and toxico- roles that allow cells to deal with changes of the logical investigations have validated the suitabilet al.- environmental constrains. For example, the diver- ity of algal biomass for use as a high-grade feed in sity of light-harvesting pigments allows efficient the production of bivalve molluscs (Kovač , Bulletin UASVM Animal Science and Biotechnologies 77 (2) / 2020 4 and al.

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et al. photosynthesis at different depths in the seawater pendent on both the energy status and the taxo- column (Heydarizadeh , 2013). nomic composition of the phytoplankton commu- Regarding lipids in aquatic ecosystems, phy- nity, with some microalgal classes being devoid of toplankton can predominantly synthesize poly- these compounds (e.g., chlorophytes have no PU- unsaturated fatty acids (PUFA), which in turn are etFAs al. longer than 18 carbons, but 20 - and 22 - car- mainly consumed by zooplankton and benthic bon FeedingPUFAs are Mechanism considered of to Bivalve be essential) (Kovač invertebrates. Different groups of phytoplankton , 2013). such as cryptophytes, diatoms, dinophytes and euglenophytes, can synthesize high amounts of Based on the mechanism of food collection, highly unsaturated fatty acids (HUFA – a subset bivalves canet beal. suspension–feeders or deposit– of PUFA), which etare al. transferred and accumulated et al. feeders, or even utilize both feeding methods at progressively higher levels in aquatic organ- (Arapov , 2010). Although there are isms (Gladyshev n , 2009; Koyande , 2019). some differences in particles processing, basic Thus, an aquatic ecosystem offers the principal mechanism remains the same. Once particles dietary sources of -3 HUFA for all aquatic ani- entered the mantle cavity, they are transferred mals. Generally, the phytoplankton fatty acids are along theet ctenidiumal. to the labial palps, which composed of saturated fatty acid (SAFA), monoun- are considered as a main site of particle selection saturated fattyet acids al. (MUFA) and polyunsaturated (Arapov , 2010). After selection on the palial fatty acids (PUFA) (including also their derivatives organs, some particles are rejected as pseudofeces HUFA) (Kovač , 2013). However, the traces of while other are ingested (Gofas, 2012). When phytoplankton in an aquatic food web remain as particles through oesophagus enter the stomach, phytonutrients, primarily providing PUFA, e.g. ei- mechanical and enzymatic decomposition of cosapentaenoic acid (EPA), arachidonic acid (AA) et ingested food begins. Rotating crystalline style al.and docosahexaenoic acid (DHA), usually supplied mechanically breaks large particles while enzymes at a higher-level in consumers (Arab-Tehrany released from the style start to decompose organic , 2012). Additionally, environmental conditions particles (Zanzerl, 2015). Food particle selection significantly influence the metabolic processes, is based on particle size, shape, nutritiveet al value or while the quantity and quality of essential micro chemical component on the surface of the particle etand al. macroelements in food and water are of para- (Lehane & Daven-port, 2006; Yahel ., 2009). mount importance for bivalve (Terech-Majewska In the Filibranchia and Eulamellibranchia, , 2016). Lipids (especially PUFA), in turn, are water is drawn into the shell from the posterior the nutritional factors and essential components ventral surface of the animal, passes upwards in modifying the animal growth, health and even through the gills, and doubles back to be expelled reproduction (Desvilettes and Bec, 2009). There- just above the intake (Taylor & Glover, 2006). In fore, phytoplankton are broadly recognized in burrowing species, there may be two elongated, bivalve mariculture as a key nutritional live food retractable siphons reaching up to the seabed, owing to its high amounts of phytonutrients and one each for the inhalant and exhalant streams of biologically active ingredients. water. The gills of filter-feeding bivalves are knownet Moving from gross measures of food quantity alas ctenidia and have become highly modified to to food quality, there is a consensus that high pro- increase their ability to capture food (Arapov tein contents in phytoplankton cells, and conse- ., 2010). For example, the cilia on the gills, which quently in seston of coastal waters, et al. generally are originally served to remove unwanted sediment, able to provide nutritional needs of bivalves for has become adaptedet toal capture food particles, and dietary protein (Arab-Tehrany , 2012). In con- transport them in a steady stream of mucus to the trast, specific lipids, especially long - chain, PUFA mouth (Cranford ., 2011). The filaments of appanand certain et al. sterols, may be limiting in phytoplank- the gills are also much longer than those in more ton and seston food sources of bivalves (Pachi- primitive bivalves, and are folded over to create , 2019). These lipids are required as a groove through which food can be transported etstructural al. membrane components in bivalve cells, (Taylor and Glover, 2006). The structure of the rather than for their energy content (Delaporte gills varies considerably, and can serve as a useful Bulletin ,UASVM 2005). Animal Dietary Science and PUFAsBiotechnologies and 77(2) sterols / 2020 are de- means for classifying bivalves into groups. 5

Bivalve Mariculture in Two – Way Interaction with Phytoplankton: A Review of Feeding Mechanism and Nutrient Recycling

Poromya granulata A few bivalves, such as the granular poromya nutrient regeneration is related to the abundance ( ), are carnivorous, eating and location of bivalves in a system. The extent much larger prey than the tiny microalgae to which this affects overall nutrient budgetset andal. consumed by other bivalves (Krylova, 2001). In thus primary production is related to the system these animals, the gills are relatively small, and flushing rate and residence time (Newell , form a perforated barrier separating the main 2005). mantle cavity from a smaller chamber through The majority of studies of bivalve effects which the water is exhaled. Muscles draw water in on nutrient recycling have focused on nitrogen through the inhalant siphon that is modified into a because this is the mostet al. common nutrient-limiting cowl-shaped organ, sucking in small crustaceans biological production in marine and estuarine and worms at the same time. The siphon can be systems (Arapov , 2010; Napiórkowska- retracted quickly and inverted, bringing the prey Krzebietke, 2017). Benthic bivalves are important within reach of the mouth while the gut is modified contributors of nitrogenet al. (usually in the form of so that large food particles can be digested (Ward ammonium, NH4+) to both subtidal and intertidal & Shumway, 2004). systems (Newell , 2005). Nitrogen is retained As the dietary energy available to a feeding within some systems through direct recycling bivalve is modified by the carbon status of the of nitrogenet from al. bivalves to phytoplankton. In phytoplankton, feeding over the course of the the Marennes-Oléron culture region in France, day will present bivalves with a range of energy Leguerrier (2004) show that higher oyster contents within ingested food (Krylova, 2001). production increased benthic-pelagic coupling, Similarly, the protein, hence nitrogen, content of which in turn increased secondary production (in phytoplankton is dependent on the availability the form of meiofauna), providing food for juveniles of this nutrient and sufficient energy for anabolic of predatory nektonic species. Also, Mazouni protein synthesis (Geider & La Roche, 2002). The (2004) demonstrates that other planktonic feeding habits and/or preferences of different organisms (bacteria, ciliates, and flagellates) can bivalve species vary immensely. However, the act as sources of nitrogen for bivalve molluscs in composition of diets ingested by the first larval the absence of suitable autotrophic phytoplankton. stages is quite similar and, in turn, very important Alteration in the concentration level of silica in assessment of the feeding conditions and remains one of the noticeable change during the opportunities to satisfy food requirements in feeding and elimination processBacillariophyceae carried out by aquatic ecosystems (Napiórkowska-Krzebietke, bivalves. It is however important to know that silica 2017). The composition of a diet is usually is a macronutrient of the class , expressdetermined the results.based on an analysis of the entire gut or the diatoms. When a bivalve consumes diatom content,Nutrient and a Recycling percentage-based Activities method of Bivalves is used to biomass, portions of the nitrogen and phosphorus components are assimilated into bivalve tissues, etand al., remaining portions are returned to the Benthic suspension feeders, such as many environment in relatively labile forms (Newell species of bivalve molluscs, influence the nutrient 2005). Complex, organic molecules in bio- and organic coupling of benthic and pelagic deposits can be recycled rapidly by bacterial systems through their ability to filter a wide size decomposition, and nitrogenous wastes in range of particles and deposit organic wastes that the form of ammonia and urea are available sink to the bottom (bio-deposition) (Wikfors, immediately for phytoplankton reuse. Silica in 2011). Suspension-feeding bivalves perform this diatom frustules, however, can be returned to the function in a range of habitats and physiographic environment in a form, the mineral opal that is conditions where they filter out and deposit only slowly remineralized under conditions found significant amounts of suspended material, as well within bio-deposits (Wikfors, 2011). Thus, Bivalve as excrete dissolved nutrients. Bivalves influence mariculture can be considered efficient recyclers nutrient dynamics through direct excretion of nitrogen and phosphorus in the environment and indirectly throughet microbiallyal. mediated while the intense feeding by bivalves can be remineralization of their organic deposits in the considered an activity that encourages the growth sediments (McKindsey , 2006). Therefore, of non-diatom Bulletin UASVM microalgae Animal Science and on Biotechnologies recycled 77 nitrogen (2) / 2020 6 and al.

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et al. and phosphorus. This is the process characterized crease the product’s market price by 40% (Muller- as the “cultivation” of a flagellate food source by Feuga , 2003). bivalve populations. In the case of the bivalve molluscs that are The positive and negative feedback mecha- suspension-feeders and the phytoplankton that nisms observed in aquatic systems as a conse- constitute a large fraction of the living component quence ofet al. nutrient dynamics mediated by mol- of the suspended section upon which molluscs luscs have been the subject of numerous studies feed, the most obvious interaction is bivalves (Newell , 2005). Their high filtration capacity, eating phytoplankton. Increasingly, however, the rapid response to high levels of food (e.g. plank- reverse trophic interaction is being recognized; ton), and relative permanence in aquatic systemset al., dissolved inorganic and organic waste compounds give bivalves the ability to stabilize systems and released by metabolically active bivalves et canal. enhance resilience to perturbations (Jackson supply phytoplankton with nutrient and energy 2001). Large bivalve assemblages can regulate the requirements for their growth (Newell , abundance of phytoplankton in shallow seas and 2005). This two-way interaction can be viewed intense filtering can reduceet al. phytoplankton bloom as a type of community symbiosis developed over intensity while extending the duration of less in- long evolutionary timescales (Figure 3). tense blooms (Ogilvie , 2000). Filtration and Also, the reef - building characteristics of some bio-deposition of phytoplankton and other sus- species, such as oysters, have served under natural pended materials by extensive beds of bivalves conditions to transfer benthic organisms into the also reduce downstream transport, thereby mod- pelagic realm where they are within the primary erating effects of excess nutrients or sedimenta- productivity maximum near the water surface tion in outlying waters. Thus, bivalves provide the and less vulnerable to stress from siltation and systemTwo-Way with a Interaction capacity to Between buffer against Bivalve sudden hypoxia (Wikfors, 2011). Oysters have long been perturbationsMariculture and Phytoplankton considered to be “ecosystem engineers” more for their reef - building activities modifying benthic valve mariculture habitat than for their trophic interactions, while Phytoplankton are a key food item in bi- until recently are the particle clearanceet al.and nutri- , where they are naturally oc- ent recycling activities of oysters being considered curring and introduced into enclosures with the in oyster restoration efforts (Coen , 2007). normal circulation of seawater. According toCras Xu- Similarly, mussels attach to any hard substrate sostreaand Yang gigas (2007), and mussel phytoplankton Mytilus galloprovincialis are the most in the environment and then to each other, form- important food source for intertidal oyster Chla- ing three - dimensional aggregations that change mys farreri , shape as byssal threads are formed and broken by as well as for the subtidal cultured scallop waves and tidal currents (Dolmer 2000; Lawrie & . However, depending on their size and McQuaid,Conclusions 2001). habitat, bivalves utilize different fractions of phy- toplankton. By analyzingC. farreri fatty acid markers, Xu and Yang (2007) foundC. gigas that and primary mussel food M. gallopro sources- The established bivalve-phytoplankton sym- vincialisof cultured scallop were diatoms, while biosis involves phytoplankton serving as a key nu- in a diet of oyster I. galbana tritional live feed in bivalve mariculture owing to Tetraselmis,dinoflagellates Chlorella, prevailed. Dunaliella, Nutrient-rich Haemato- its high amounts of phytonutrients and biological- coccus,microalgal Chaetoceros, strains of Skeletonema,and Thalossiosira,some genera ly active ingredients (fatty acids, amino acids, ca- Naviculalike Amphora rotenoids, chlorophyll, vitamins, antioxidant) and bivalves serving as consumers and cultivators of , are cultured widely for bivalve phytoplankton owing to their feeding mechanism mariculture (Shields, 2012). Another example of and nutrient recycling activities. Feeding with the use of phytoplankton in bivalve maricultureHas is- wide range of food sources bivalves directly influ- leaa conventional ostrearia French approach called the green- ence not only phytoplankton community but also ing of oysters. This includes using the diatom bacterioplankton and zooplankton communities. to obtain a blue coloration on the gills Bivalve mariculture can restore trophic balance Bulletinand labial UASVM palpAnimal ofScience oysters. and Biotechnologies This was 77(2) reported / 2020 to in- between the bivalves and phytoplankton commu- 7

Bivalve Mariculture in Two – Way Interaction with Phytoplankton: A Review of Feeding Mechanism and Nutrient Recycling

Figure 3.

“Box model” of a suspension - culture, oyster nursery, with arrows depicting exchanges of carbon, nitrogen, and phosphorus between the oyster nursery and environmental compartments. Of particular note are the arrows indicating return of respiratory carbon (CO2) and excreted nitrogen (NH4+) to the phytoplankton community, thereby recycling resources not assimilated immediately by the oysters. (Source: Wikfors, 2011)

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