OPEN ACCESS

International Journal of Aquatic Science

ISSN: 2008-8019
Vol. 8, No. 2, 69-77, 2017

-Review-
Nutritional importance for aquaculture and ecological function of
microorganisms that make up Biofloc, a review
Daniel Becerril-Cortés1, María del Carmen Monroy-Dosta2, Mauricio Gustavo Coelho-Emerenciano3, Germán Castro-Mejía2, Kathia Cienfuegos-
Martínez1, Ramón de Lara-Andrade2

1) UAM-Xochimilco, Maestría en Ciencias Agropecuarias, Mexico.

2) UAM-Xochimilco, Laboratorio de Análisis Químico de Alimento Vivo, Mexico.
3) Universidade do Estado de Santa Catarina (UDESC), Laboratório de Aquicultura (LAQ) y Laboratório de Nutrição de Organismos Aquáticos (LANOA),
Brasil.

Received: May-12-2017 Accepted: July-07-2017 Published: July-28-2017

Abstract: The objective of this review is to provide an overview of the nutritional importance and ecological function of microorganisms in
Biofloc systems. For the elaboration of this review different databases were consulted, principally, PubMed, Scopus, Web of Science and
Scielo. First, it is described the interactions between bacteria and phytoplankton in Biofloc, which are important for maintenance of water
quality, because they are involved in transformation of organic matter and a better removal of contaminant residues such as nitrogenous
compounds. Also, these organisms are important for aquatic ecosystems because they are an essential component of trophic nets in activity
and biomass quantity, contributing to regeneration of nutrients and interacting with many organisms serving as base of food chain.
Subsequently, mention is made of relevance of zooplankton that develops in Biofloc culture systems, because they represent a key role in
animal’s nutrition in culture and have proven benefits in growth rates, in food conversion factor and reduction in costs associated to
commercial food.

Keywords: Heterotrophic bacteria, phytoplankton, aquaculture nutrition, zooplankton

Introduction
Nowadays, aquaculture production systems have energy source, that through of redox process they
been transformed to solve different activity produce less complex chemical forms and nitrogen
problematics, as use of large quantities of water, from food wastes, that are used for proteins synthesis
contamination of tributaries discharge and (Azam et al., 1983), which results in a micro trophic
dependence in feeding meal in formulated diets net, where several ecological relations are carried out
(Hernández-Barraza et al., 2009). Regarding to alime- (commensalism, competition, predation among
ntation, it is important to point out that in production others), in a community constituted by bacteria,
units, large quantities of formulated food of high price microalgae, ciliates, rotifers, crustaceans and
are used, which represents 40% of production costs nematodes which are available whole day as natural
(FAO, 2005). In addition, in most cases, commercial food for cultured species (Avnimelech and Kochba,
diets do not cover all nutritional requirements of 2009; Emerenciano et al., 2013). Different authors
species or include protein contents superior to agree that there are some advantages of the Biofloc
necessary and cause low digestibility, palatability, and system compared to conventional farming systems.
water stability, that up to 60% of food that is supplied it These advantages are: lower investment costs, good
is not used by organisms in culture and when it use and maintenance of water quality during
decompose it compromises water quality (Martínez- cultivation, pathogen control, high crop densities and
Córdova et al., 2002; Tacon et al., 2004). benefits associated with the feeding of cultivated
Because of this, one production systems that has organisms, as well as reduced costs associated with it
attracted attention in recent years is Biofloc (Avnimelech, 2009; Crab et al., 2012; Hargreaves,
technology (BFT), which consist in generation of 2013).
microbial flocs, using an external carbon source, This cultivation technique allows to work with a
which is available in water and used by bacteria as much smaller investment than the traditional systems,

() [email protected]
 Becerril-Cortés et al. (2017) Nutritional importance for aquaculture and ecological function of …

because bio filters, pumping, solids filtration and water minerals. Therefore, microorganisms associated with
disinfection are not used and without considerable biofloc play a key role in nutrition of animals in
water inputs throughout the crop, thus providing an cultivation since they are a rich natural source of
advantage over the use of water resources, being a protein-lipid "in situ" available 24 hours a day, with the
more economical alternative, reducing water above, it is known that the potential feed gain with this
treatment costs by up to 30% (Crab et al., 2012). technology is 10 to 20% due to that the costs per
It is recognized that the normal operation of the feeding decrease between 40 to 50% (Hargreaves,
ponds may include the replacement of water (usually 2013), the nutritional quality of Biofloc is considered
10% per day) as a method to control the quality of the good for the cultivation of aquatic organisms since it
liquid. In contrast Biofloc systems can operate with a has been reported that it can contain between 25 and
low water exchange rate of 0.5 to 1% per day, while 50% of protein and up to 0.5 to 15% of fats, however,
maintaining sufficient aeration to maintain suspended this content may vary in relation To the carbon source
flocs, reduce pumping costs, preserve nutrients in used to promote Biofloc, the planktonic community
tanks and the volume of the effluents is reduced that develops in the system and the cultivated species
(Gaona et al., 2011; Ray et al., 2011), with the use of (Ekasari et al., 2014b; Emerenciano et al., 2013).
this type of systems reduces the discharge of Despite many benefits, the Biofloc system also has
pollutants and diseases to the wild, on the other hand some disadvantages to take into account, for
working with high crop densities reduces the example, the need for a start-up period, the
ecological footprint of cropping systems, thus investment required for an aeration system to ensure
contributing to the conservation of ecosystems the maintenance of suspended solids, cyanobacteria
(Krummeanuer et al., 2011). About the maintenance blooms and the accumulation of nitrogen compounds,
of water quality, this is mediated by the bacterial as well as another limitation to increase the use of this
community and this is achieved by using a high type of crops is that, being a system with zero water
carbon to nitrogen (C:N) ratio to ensure the best change, the water becomes cloudy so there is a
growth of heterotrophic bacteria by applying an resistance on the part of the farmers for a
external carbon source. The heterotrophic bacteria misconception that the crop water must always be
are responsible for capturing nitrogenous compounds clean (Hargreaves, 2013).
released by the fish and use them in their growth, thus It has been documented the need of use of live
eliminating ammonium and nitrite toxicity (Azim and food organisms in of aquatic production, mainly in
Little, 2008; Nootong et al., 2011). larvae stages, because they provide higher diversity
Regarding the control of pathogens, Crab et al., of nutrients, are easy to assimilate and more attractive
(2010) mention that in this type of culture systems, for cultured species (Wasielesky et al., 2006). Even
bacteria with probiotic potential are developed, this though, in last years, studies have been published
can be due to the fact that, in the feces, part of the about positive effect in growth of fish and crustaceans
intestinal microbiota is released, and being in a cultured in Biofloc, few studies have been made to
nutrient medium, it is possible that the cultivated characterize developed planktonic communities, their
species take advantage of the benefits that these importance as food and ecological function in
microorganisms provide, some of these benefits are: production productive systems. Because of this, it
increase in the immune response against infectious must be made a review that allows to have a broader
processes and better assimilation of nutrients by the picture of planktonic groups that develop in Biofloc
cultivated species, which leads to their greater culture systems, their importance as natural food for
survival and growth, likewise, probiotic bacteria cultured species and the ecological role they have in
participate in a process of competitive exclusion the system.
because they generate a hostile environment to
pathogenic bacteria by the excision of exoenzymes Biofloc system characteristics
and polymers that release in the aquatic environment Biofloc is an intensive production system in
(Monroy-Dosta et al., 2015). aquaculture, which can overcome difficulties of
As for the benefits associated with food, these activity, such as increase in biomass per volume of
can be attributed to the fact that microbial aggregates water and use of less water, overcoming paradigms of
can provide important nutrients such as sustainability (Avnimelech, 2009). The term “floc” or
carbohydrates, proteins, amino acids, fatty acids and “Biofloc” can be defined as flocculation of organic

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 Becerril-Cortés et al. (2017) Nutritional importance for aquaculture and ecological function of …

matter present in medium, resulting in a high BFT has been used on different aquaculture
concentration of biomass in form of particles or species. Table 1 summarizes some studies and show
bioflocs (Cuzon et al., 2004; Emerenciano et al., the different carbon sources that have been used in
2011). This term applies to a compound consisting of these, besides briefly explain the objectives of the
60 to 70% of organic matter, which includes an study and the main results
heterogeneous mix of microorganisms (fungi, algae,
bacteria, protozoans, and rotifers) and 30 to 40% of Diversity of microorganism associated to
inorganic matter such as colloids, organic polymers,
Biofloc
cations and death cells (Fig. 1) (Chu and Lee, 2004).
The diversity of organisms that make up bioflocs are,
bacteria, microalgae, yeast, rotifers, ciliates,
protozoans, nematodes, and crustaceans (Monroy et
al., 2013; Collazos and Arias, 2015), this biodiversity
of species, depends on carbon source and cultured
specie (Ray et al., 2010).
In these bioflocs, both autotrophic and
heterotrophic activities occur, also aerobic and
anaerobic processes from which key interactions
emerge for water quality maintenance, as control of
nitrogenous compounds (Ray et al. 2010; Ebeling et
al., 2006). Microorganisms are an essential part of
aquatic ecosystems because of their place in trophic
webs in marine and freshwater environments both in
activity and biomass quantity, contributing to nutrient
regeneration and interacting with a wide range of
Fig. 1: Biofloc observed with an optical microscope a) organisms (Monroy et al., 2015). Three main groups
Microalgae and Vorticella sp. (40x); b) Vorticella adhered to of microorganisms associated to Biofloc are
a floc (10x); c) Rotifer of the genus Lecane and recognized, these are bacteria, phytoplankton, and
Cyanobacteria species. (10x) (Own source) zooplankton.

Tab. 1: Summary of different studies carried out with biofloc technology.

Species CS Objective Main result Ref.
Evaluate effect of different carbon They suggest that the choice of the carbon source
Macrobrachium. Acetate,
sources on the nutritional value of used for biofloc culture influences its nutritional 1
rosenbergii glycerol
bioflocs, as feed. value.
Estimate the effect of producing Indicated that Biofloc positively affects nile tilapia
Oreochromis.
Molasses and culturing nile tilapia larvae in larvae performance, in terms of larval growth 2
niloticus
Biofloc. performance and robustness.
They mention that intermediate levels of bioflocs
(TSS between 400 and 600 mg L−1) may be
They tested the effect of three
suitable to superintensive culture and suggest that
Litopenaeus. concentrations of bioflocs in the
Molasses ammonia and nitrite in T400-600 and T800-1000 3
vannamei culture, water quality and
tanks were mainly controlled by nitrifying bacteria,
performance of shrimp.
which provided greater stability of these
parameters and of dissolved oxygen.
Suitability of biofloc whit diferents The study demonstrates thatdietary
Penaeus. leves of inclusion of dried biofloc, supplementation of biofloc at 4–8% level had
Wheat flour 4
monodon as dietary supplement in shrimp beneficial effects on growth performance and
feed digestive enzyme activities.
Investigated the effectiveness of BFT offers the possibility to simultaneously
bioflocs technology for maintaining maintain a good water quality and produce
Marsupenaeus
Sucrose good water quality, supplying feed additional food for shrimp, besides microbes 5
japonicus
nutrition and inhibiting potential detected in bioflocs could be useful in resisting
pathogens. disease in high-intensive shrimp farming systems.

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Tab. 1: Continued
Species CS Objective Main result Ref.
They investigated the effect of They report an increase in the growth and welfare
biofloc system, on inorganic of the fish cultivated, which can be attributed to the
Labeo rohita Molasses 6
nitrogen control, growth and in situ maintenance of water quality within the
immunological response of rohu. biofloc system and the presence of microbial flocs.
CS = Carbon sourse employed
Ref.: 1) Crab et al. (2010), 2) Ekasari et al. (2015), 3) Schveitzer et al. (2013), 4) Anand et al. (2004), 5) Zhao et al. (2012), 6) Kamilya et al. (2017)

Bacteria
Bacteria and unicellular fungi are important for compounds is more efficient, because this process is
aquaculture production systems because they act in a carried out by bacteria of Bacillus and Pseudomonas
positive way in organic matter transformation, removal genders (Monroy et al., 2015). Also, presence of
of contaminant compounds and as a source of organic matter as carbon, inhibits denitrification by
microbial biomass available for larger organisms (De autotrophs, so they grow up slowly compared to
Scryver et al., 2008). heterotrophic, that increase their population faster in
Heterotrophic bacteria, is the most important water with high content of organic matter and high
bacterial group in Biofloc system their growth is oxygen concentration, so they can transform
involved in a better removal of contaminant ammoniacal nitrogen into low toxicity compounds;
compounds, through their metabolism. These bacteria even some of them, transform this compound to
release many inorganic compounds to environment produce microbial biomass and allow generation of
that can be used by other organisms and produce diverse protozoans in a short time (days) compared to
exo-enzymes which decompose diverse compounds conventional systems (Ebeling et al., 2006). Studies
as cellulose, lignin, keratin, and other natural where they have a more specific characterization on
molecules that are hard to transform. The processes bacterial genus or species in Biofloc are few, some of
of denitrification and decomposition will not be carried them are resumed in Table 2. In addition to its
out so effectively without the involvement of ecological function, these bacteria can be used as
heterotrophic microorganisms (Avnimelech, 1999), unicellular or microbial protein (SCP or Single Cell
these microbial groups reduce impact through Protein) and can provide important percentages of
removal of ammoniacal nitrogen by nitrification protein (40-80% of raw protein in dry basis, depending
process that consists in successive oxidation of on specie) (Tacon, 2013), and therefore they can be
ammonia first to nitrite and finally to nitrate. In Biofloc considered as a supplement for fish and shirmps
systems, transformation of toxic nitrogenous larvae (Palmerin et al., 2012).

Tab. 2: Description of bacterial groups reported in Biofloc systems by different authors.

Marine or freshwater
Reported bacterial group Ref.
specie employed
Reported the different
Indicated the presence of genus such as Pseudomonas, Bacillus,
bacterial groups that can be 1
Alteromonas and Micrococcus, Cellulomonas, Clostridium
found in Biofloc
They report predominant bacterial communities, such as
Marsupenaeus japonicus Proteobacterium, Actinobacterium, Bacillus sp., Roseobacter 2
sp.and Chytiphaga sp.
Reported bacterial phyla such as Proteobacteria, Bacteroidetes,
Litopenaeus stylrostris 3
Cyanobacteria, Planctomycetes and Verrumibrobia
Reported genus of probiotic and degradative bacteria:
Oreochromis niloticus Lactobacillus Burkholderia, Lactococcus, Saccharomyces, and 4
Bacillus among others
Employed fresh pond water
Reported the presence of different phyla: Firmicutes,
to inoculate the tank with 5
Protobacteria, Actinobacteria, Acidobacteria
natural microorganisms
Reported mainly pathogen species such as: Vibrio rotiferianus,
Litopenaeus vannamei Photobacterium jeanii, Photobacterium damselae, 6
Pseudoalteromonas spongiae, Vibrio mytil
Ref.: 1) Monroy et al. (2015), 2) Zhao et al. (2012) , 3) Cardona et al. (2016) , 4) Maya et al. (2016), 5) Wei et al. (2016) ,
6) Luis-Villaseñor et al. (2015)

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Phytoplankton microalgae-bacteria relation as determinant of groups

Another important group in Biofloc systems is develop in aquatic environments, in such a way the
phytoplankton, microalgae use ammonia, and increment of carbon-transforming heterotrophic
compounds as nitrite and nitrate for construction of bacteria, make possible an increase of diatoms in
proteins and sugars, and they also provide oxygen system and restrict other groups like cyanobacteria,
during day time. Diverse phytoplankton species, like that are potentially harmful in aquaculture systems
diatoms, are nutritive and can improve the production because they can form superficial layers that adhere
of cultured species as prawn culture, due to its to fish gills causing mortality, also some genus as
contributions of essential amino acids and highly Anabaena sp. and Ocillatoria sp. have capacity to
unsaturated fatty acids (Moss, 2002). produce toxic metabolites that can increase in case of
Genus and species reported by various authors exponential growth (Monroy et al., 2013; Massaut and
are; Scenedesmus quadricauda, Coelastrum sp., Ortiz, 2003).
Pediastrum dúplex, Cyclotella sp, Navicula sp,
Synedra sp, Fragilaria sp, Fragilaria, Orthoseira, Zooplankton
Rhabdonema, Ulothrix, Skeletonema, Cylindrotheca, In aquaculture production systems with Biofloc,
Hemiaulus, Phymatodocis, Ulothrix, Cyanobacteria diverse planktonic groups develop in a natural way,
Chlorophyta, Bacillariophyta, Euglenophyta and such as rotifers, protozoans (ciliates and flagellates),
Dinophyta, (Ferreira and Otavio 2014; Castro et al., crustaceans and nematodes which play an important
2014; Monroy et al., 2013; Brito et al., 2013). role in nutrient recycle, maintenance of water quality
Nutritional value of microalgae, is related to the and in nutrition of cultured animals (Emerenciano et
environment in which they develop and inorganic al., 2013). Consumption of zooplankton present in
compounds they use for growth. The composition of Biofloc has shown countless benefits, such as
carbohydrates, regarding to specific sugars, can improvement of growth rate, increase in food
considerably variate between algae species. conversion factor and benefits costs associated to
Generally, glucose is found in higher concentrations, balanced food (Hargreaves, 2013). Proximal
followed by galactose, mannose, and ribose. composition of some planktonic species that are found
Nutritional values of some microalgae species are in bioflocs, indicate that rotifers can contain between
shown in the Table 3. According to Fernandez-Reiriz 54 and 60% of raw protein, while cladocerans 50-68%
(1989), green microalgae have low concentrations of and copepods 70-71%, regarding lipid values in
monounsaturated fatty acids and high concentrations rotifers, they contain from 3.9 to 13.2% depending on
of polyunsaturated that are of great importance for specie, cladocerans have between 1 and 2.9% while
growth of fish and crustaceans. copepods can contain up to 2.6% of lipids (Ray et al.,
2010), while nematodes are 76% water and 24% dry
Tab. 3: Nutritional values of micro algae according to the matter; 40% of dry matter is protein and 20% fat,
authors cited. remaining 40% correspond to nitrogen-free extract
and other macronutrients (Figueroa, 2009).
Carbohydrate
Species

Protein

Lipids

Ref.

Nutritional contributions of Biofloc

The carbon source is the main input for Biofloc system
Freshwater operation, so selection of this source can cause
24.1 2.47 n/a 1
Scenedesmus variation in nutritional value and taxonomic
Marine Dunaliella 38.3-52.8 7.7-10.8 8.4-12.7 2
Marine Chlorella sp. 16.6-35.8 13.6-15.3 22.6-54.5 3
composition of bioflocs (Crab et al., 2012). Maicá et
Marine P. lutheri 16.02-52.35 12.39-37.83 15.63-53.10 4 al. (2012) using molasses as carbon source reported
Values represented in percentage, n/a = Not available protein values of 28.7 to 43.1% and lipids between
Ref.: 1) Andrade et al. (2009), 2) Suárez et al. (2007), 3) Paes et al. (2015), 4)
Fernandez-Reiriz, (1989) 2.11 and 3.62% in bioflocs used to culture L.
vannamei. In tilapia cultures using wheat flour protein
Therefore, today different microalgae are levels of 38% and lipid values between 3.16 and
specifically used in aquaculture, taking into 3.23% (Azim and Little, 2008). Emerenciano et al.
consideration their nutritive inputs and its ecological (2011), reported values of protein of 30.4%,
importance because they are base of all aquatic food carbohydrates of 29.1% and lipids of 0.5% in a system
chains (Muller, 2000). There is an important adding molasses; Crab et al. (2009), used acetate,

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 Becerril-Cortés et al. (2017) Nutritional importance for aquaculture and ecological function of …

glycerol and glucose as carbon source finding values found that their composition presented acceptable
between 42 and 58.9% of protein in dry weight in their values of proteins and lipids. Other evidences of
different treatments; López Tarín (2011) made a nutritional contributions that Bioflocs can contribute
tilapia culture in closed system, partially substituting are shown in Table 4.
formulated food with bioflocs with molasses, and

Tab. 4: Bromatological composition based in bioflocs dry matter and compared

with commercial food for fattening stage.
Carbon source RP (%) Carb (%) Lipids (%) RF (%) Ashes (%) Ref.
Starch 31.5 n/a 85.2 n/a 12.4 1
Saccharose 49 36.4 1.13 12.6 13.4 2
Unrefined granulated sugar 23.7-25.4 32.2-39.1 2.6-3.5 n/a 33.0-40.4 3
Molasses with cornmeal 23.5-32.3 n/a 2.9- 5.33 n/a 20 - 36 4
- 25-35 n/a 5-7 3-6 5-12 5
- 30-35 n/a 5-7 4 11-12 6
RP= Raw protein, Carb= Carbohydrates, FB= Raw Fiber, n/a= Not available
Ref.: 1) Wei et al. (2016), 2) Kuhn et al. (2009), 3) López et al. (2014), 4) Wang et al. (2016), 5) Commercial food for
tilapia (Alimentos del Pedregal®), 6) Commercial food for shrimp (Alimentos del Pedregal®)

Benefits of these nutritional inputs are reflected in present in Biofloc develop is important, nevertheless,
higher growth rates, survival, improvement in food is still unknown in its totality, so it is suggested to
conversion factors and general well, being in cultured carry out more studies that characterize species
species. Regarding this, Azim and Little (2008) in a diversity, both bacterial and planktonic that can be
Nile Tilapia Oreochromis niloticus culture, in Biofloc present in Biofloc systems and that help to explain
system, reported a production 45% higher in this interactions that are carried out in this type of
system compared to traditional system. Sierra-De la aquaculture farming systems.
Rosa et al. (2009), presented good growth rates (500
g/226 days; 2.1 g/day), survival of 70% and better Acknowledgments
food conversion factor (1.5) in a study with tilapia. First author thanks Postgraduate Program: Master in
Agricultural Sciences of Universidad Autonoma
Conclusions Metropolitana for provided support. Also to Consejo
Nutritional quality contributed by microorganisms Nacional de Ciencia y Tecnología (CONACyT) for
associated to Biofloc is comparable and/or superior granted scholarship, number CVU 763361.
regarding to commercial food in terms of protein and
fats, also they contribute and adequate content of References
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