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LOOKING AHEAD TO 2021
VOL. 45 2 SEPTEMBER 2020
An update on our
AE2020 and 2021 CORK, IRELAND APRIL 12-15
events next year
A Norwegian Portal for
aquaculture sustainability
Phage therapy for
seabass/seabream Madeira, Portugal Oct. 4-7
T H E M E M B E R S ’ M A G A Z I N E O F T H E E U R O P E A N A Q U A C U LT U R E S O C I E T Y 2nd Semester 2020
Afgiftekantoor: 8400 Oostende Mail
AQUACULTURE
VOL. 45(2) September 2020 EUROPE
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promoting contacts
From the EAS President............................................................ 4 among all involved in aquaculture. EAS was
founded in 1976. Aquaculture Europe is the
members’ magazine of EAS.
FEATURE ARTICLE Secretariat
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The prospect of phage therapy
in fish hatcheries.................................. 9 Madeira Cliffs, Board of Directors (2018-2020)
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President: Gavin Burnell (Ireland)
Biofloc Based Fish Farming (BFT): A new
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aquaulture in India................................................................... 14 Past-President: Bjørn Myrseth (Norway)
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Aquaculture Europe • Vol. 45(2) September 2020
3
FRO M TH E E AS PRES I D ENT
I was looking forward to handing over to Herve Migaud, the next President of EAS, at our
annual conference. This was to have been held in Cork this autumn. Instead the world has
been turned upside down by the Covid-19 pandemic and therefore we will now have an
online General Assembly on September 30th when he will take over. These are challenging
times for the society and one of the biggest areas for concern is the loss of revenue from
our annual conference. Even although this year’s event has been rescheduled for Cork in
April 2021 and we still have the AE2021 meeting in Madeira in October 2021, it is not yet
clear how attendance will be. The majority of booths at both events have however, already
been sold, so that is a positive sign. That of course assumes that they both take place. Most
airlines have taken a big hit and experts are predicting that it will be 2022 until we get some
degree of normality back into international travel. The same experts seem fairly confident
that we will get a vaccine next year and this scenario seems to be the only one that allows
widespread international travel and large indoor meetings to take place.
The EAS peer reviewed journal, Aquaculture International has recently undergone some
Gavin Burnell changes which I would like to highlight. Since January this year you may have noticed that
President we have taken on 5 Associate Editors who all bring their own expertise to the journal. In
no particular order they are Professor Brian Austin (Disease and Health), Professor Pierre
Boudry (Genetics), Professor Michael Hartnett (Engineering and Environment), Professor
Elena Mente (Crustaceans) and Dr Ronan Sulpice (Micro and Macroalgae). This has not
only considerably expanded the areas of expertise covered by the journal, but has also taken a
lot of the administrative weight off my shoulders.
Next month in the journal we will also be expanding an exciting new feature, Topical
Collections. The idea was to stimulate the submission of high quality papers and reviews
on several cutting edge topics that we had identified. After a successful 6 month trial period
with the topic Aquaponics (curated by Simon Goddek and Hendrik Monsee) we will
be extending this section to include: Innovations in disease control and diagnosis (Brian
Austin), Epigenetics in aquaculture (Pierre Boudry and Steven Roberts) ), and Smart agro-
ecological processes for crustacean farming (Elena Mente). Judging from the increase in
excellent aquaponics papers during the trial period we should soon be receiving quality
contributions on all these topics. As you can see from the following short CVs, the curators
of the topics are well qualified to lead the journal forward into a new more provocative era.
Elena Mente, Professor of aquatic animal nutrition and physiology at University of
Thessaly, Greece and Honorary Research Fellow at the University of Aberdeen, UK.
She was awarded three competitive Fellowships, two European and one from the UK, on
research on aquatic animal nutrition for aquaculture. She has more than 20 years’ experience
in research on sustainable aquaculture, crustacean nutrition and aquatic animal gut
microbiome. She has authored/co-authored/edited five books (two in Greek), more than 70
peer-reviewed papers and ten chapters in books.
Professor Brian Austin is a microbiologist with a long history of research in fish diseases,
emphasising the diagnosis and control of bacterial fish pathogens. He has researched the
taxonomy of pathogens, their diagnosis by serology and molecular methods, and control
by vaccines, probiotics and medicinal plant products. Until 2015, he was Director of
the Institute of Aquaculture and Professor of Microbiology at the University of Stirling.
strategies based on vaccines, probiotics and medical plant products. He has published over
300 scientific articles and 20 books, to date.
Pierre Boudry is a French geneticist working at Ifremer (National Institute for Ocean
Science). Since 1994, Pierre’s research is dedicated to genetics and genomics of marine
bivalves. Most of his research is connected with aquaculture or conservation issues and has
led to over 150 publications, resulting in his designation in a bibiographic analysis as the
most productive author in of oyster research worldwide from 1991 to 2014. Based in Brest,
he is leading Ifremer's Research Unit Functional Physiology of Marine Organisms and is
Associate Director of the joint research unit LEMAR – Marine Environmental Sciences
Laboratory.
Steven Roberts is a comparative physiologist with a particular interest in functional
genomics as it applies to aquaculture. For the past decade he has been studying epigenetic
mechanisms, primarily DNA methylation, in marine invertebrates including oysters and
clams. He has published over 70 scientific articles and contributed two book chapters.
Steven is an Associate Professor and the Associate Director of the School of Aquatic and
Fishery Sciences at the University of Washington, USA.
continued on page 6
Aquaculture Europe • Vol. 45(2) September 2020
4
FE ATURE ARTIC LE
EAS events in Cork
and Madeira in 2021
AN UPDATE
You will probably have seen that there will be no Aquaculture Europe event this year.
However, EAS will organise two events in 2021. AE2020 in Cork, Ireland from April 12-15 and
AE2021 in Funchal, Madeira, Portugal 6 months later from October 5-8. Here’s the latest update.
Cork, Ireland
April 12-15, 2021
#AE20CRK
AE2020. Cork, Ireland April 12-15, 2021
There is now a momentum in all aspects of food production The AE2020 Opening Ceremony, conference plenary and
towards a circular economy whereby we no longer regard Student Spotlight Award will take place on Monday, April
waste as a problem to be disposed of, but instead look 12th at 6pm in the Cork City Hall. We have one plenary
for ways to make it a resource which can be re-used at AE2020 and it will be presented by Pedro Encarnação,
- thereby closing the loop on aquaculture inputs and outputs Director Aquacultura at Jerónimo Martins Agri-Business.
and reducing environmental impact.
His presentation
Aquaculture can take the lead in the Blue - Green Bio- “Vertical Integration –
Economy and is well placed to lead by example with new Securing supply, quality
technologies such as land-based marine aquaponics, large- and sustainability: The
scale recirculating marine farms and innovative, integrated JMA fish case” will cover
freshwater initiatives on brown field sites. When it comes vertical integration in
to having a societal impact, recent research has shown that the supply chain, going
aquaculture products, from seaweed to salmon, should be from farm to the grocery
included as part of a balanced diet from the first 1000 days store, but also projects
right through to promoting healthy ageing. of circular economy,
using the food waste
This conference will bring together stakeholders from from supermarkets to
many diverse disciplines to discuss and debate cross cutting produce insect meal that
issues such as new circular economies, life-long health and can be used to feed fish Pedro Encarnação
environmentally sustainable production. The conference production. His company
parallel sessions will address the overall topic and abstract is also focusing on locally produced fish products or placing
submission is now open at the AE2020 web site www. production close to markets so as to increase the freshness of
aquaeas.org the fish and reduce the carbon footprint.
AE2020 will take place in Cork, at the Clayton Hotel Silver Pedro Encarnação is an aquaculture expert with extensive
Springs Congress Centre, from April 12 to April 15, 2021. experience around the world. He has a bachelor’s degree in
The Silver Springs is 5km from Cork city centre and shuttle Marine Biology and a PhD in Fish Nutrition. In 2005, he
buses will be provided morning and evening to transport moved to Asia as Technical director for Biomin (Biotech
delegates. in animal nutrition). After 10 years in Asia, he returned
to Portugal to join the Jerónimo Martins Agri-Business
continued on page 7
Aquaculture Europe • Vol. 45(2) September 2020
5
FEATU RE A RTI C LE
President's message
STRONG ENOUGH continued from page 4
TO FACE EVERYTHING!
These are not the only changes which are influencing
our journal. After 8 years as the publishing editor of
Aquaculture International, Alexandrine Cheronet
has moved to a new position within Springer Nature
and will head the Earth and Environmental Sciences
editorial group. She has done an excellent job over
the years helping to increase the Impact Factor of the
journal and many of you will have met Alex on the
EAS stand at our AE events. We wish her well in her
new appointment. She is replaced by Mariana Biojone
Brandão, who is heading Springer Nature Publishing
Development in Latin America and is based in Sao
Paulo, Brazil. She is an experienced editor who has
been working with Springer for many years. I remain
as Editor-in-Chief and look forward to working with
her.
In this issue of the magazine we have a compilation
of adopt a student testimonials, an article on phage
therapy by Pantelis Katharios who recently gave an
excellent EASTalk webinar on the subject, an overview
of sustainability indicators for Norwegian aquaculture
on a new portal and a visit by EAS staff member Ana
Viskovic to tuna farms in Croatia. That very neatly
gives me 2 relevant topics to talk about in this editorial.
First of all there is the “Adopt a Student” scheme
which I am delighted to report is gaining momentum
with 12 students currently receiving mentorship and
another 3 that have already been through the scheme.
As you will read in their testimonials their experiences
have been very rewarding so far. I should also add that
from my personal experience this is just as satisfying
for the mentors. Once again, I would encourage any
experienced aquaculturists from industry or academia
who might be interested in acting as mentors, to
Leiber® Beta-S – get in contact with Alistair, Ana or myself to learn
more about what is involved. Secondly, there are the
β-glucans for: webinars which have proved to be a big hit with our
members. So far Ana has organised 16 of them and they
are all available in the members’ section of our website for
Improvement of the cellular & you to see. Altogether, more than 1500 people have logged
humoral defence mechanisms on and listened to these both informative and entertaining
presentations. They are also openly available on our
YouTube channel for one month after the webinar date,
Support of immunological and total views of those videos total more than 3000. The
competence in larval & EASTalk series also includes podcasts, and to date 5 of these
have been recorded for EAS members to listen to. However,
juvenile stages we need more volunteers for a webinar or podcast, so if you
have a topic that you would like to share with our EAS
community, then please get in touch with Ana.
Improvement of feed conversion
For my final words I would just like to thank everyone
who supported and advised me during my Presidency. As
with any international organisation there is a large team
involved and in the case of our society this would include
Alistair, Linda and Ana in the office, the entire Board of
EAS and Mario and John - the conference team. Altogether
you have made EAS a very successful enterprise and I am
honoured to have guided it through the last 2 years. Over
to you Herve!
leibergmbh.de
Aquaculture Europe • Vol. 45(2) September 2020
6
FE ATURE ARTIC LE
2021 update continued from page 5
division as their Aquaculture
Director to develop the
group expansion in this new
area. He is now focussing
on developing aquaculture
projects to supply the wide
group supermarket network.
The Aquaculture Europe
events are all about
communication with the
sector. AE2020 will feature
a special international trade
exhibition, where Irish and
international companies will
present their latest products
and services. Standard and
Corner booths are available
and each booth is 6m2 (2x3m)
EAS thematic groups also organise special sessions and/or
and features walls, carpet, two chairs and one table, spotlights,
workshops within AE2020. Other industry panels will take
one power outlet, fascia identification sign and two free full
place around the trade exhibition, and technical tours will be
delegate registrations for the conference. Additional staff can
organised.
register through the booth contract at significantly reduced
rates. A special forum will be arranged for students attending
AE2020 to enable networking and exchange of ideas. The
The AE Industry Forum is a place where presentations forum will have a dedicated programme and include a special
and panel discussions focus on relevant and timely issues student reception. Students receive the full registration
for the sector. The Industry Forum in Cork will put the package plus the student reception. To qualify for the student
emphasis on cold water marine species and is being organised rate, a copy of your student I.D. is required.
in cooperation with the Aquaculture section of the Irish
Farmers’ Association (IFA) and AE2020 Silver Sponsor, A NEW FEATURE of AE2020 will be the organisation of
Bord Iascaigh a 1 day RAS@EAS workshop to be held on Monday, April
Mhara (BIM). It 12th just before the main event. To complement the science
will be held all presented in the parallel sessions of the AE conference,
day on Tuesday, RAS@EAS looks to take a different approach, with the
April 13th. The emphasis on bringing together key figures from science and
programme industry to focus on key issues, present the latest knowledge
is under and share experience with different species and systems.
development. Each RAS@EAS event will focus on a specific challenge in
RAS systems, with several sub-sessions based on interactive
Since 2019, the AE Innovation Forum looks to help discussion and audience participation.
accelerate new companies with innovation potential within
the aquaculture sector. EAS is teaming up again with
HATCH BLUE to organise a full day event on Wednesday,
April 14th. The event will feature short presentations
and pitches from (young) companies selected through an
application process.
As we move forward to develop the programme, we are
specifically interested in attracting applications from new
companies with innovative ideas and projects that they would
like to pitch during the Forum and hearing from investors
interested in supporting promising aquaculture initiatives. The event in Cork takes the theme “Creating an Optimum
Applications to pitch can be sent to EAS through this Environment”, organised in three sessions addressing these
link. The deadline is December 31 this year and successful key questions – How do we best approach disinfection?
applicants will be informed by end January latest. The full Where are we going with monitoring & autonomy? And
programme will be available early next year at the AE2020 What are the most problematic interactions between fish
web page. & their environment? Each session will have an introductory
The AE event is a focal point for meetings of European presentation, followed by a moderated panel discussion.
associations, satellite workshops of EU projects and other Registration for this event can be made separately, or included
events. We can provide options for your meeting. The in the full AE2020 registration package.
continued on page 8
Aquaculture Europe • Vol. 45(2) September 2020
7
FEATU RE A RTI C LE
Madeira, Portugal October 4-7, 2021
CONFERENCE - ae2021@aquaeas.eu
#AE21MAD TRADESHOW & SPONSORSHIP - mario@marevent.com www.aquaeas.eu
AE2021. Funchal, Madeira, Portugal. October 4-7, 2021
Europe faces important societal challenges arising from
global environmental and social-economical threats. These
include climate change, depletion of natural resources
including water and energy, pollution, food security and
safety and human migrations. But Europe, and particularly
the European Union, is also in the forefront in facing these
challenges with innovative policies regarding environmental
protection, sustainable use of living resources, marine and
coastal planning and leading technological developments and
innovation. We look forward to
Aquaculture has a clear place in securing food production welcoming you to
in Europe and presents “Oceans of Opportunities” for Cork and to Madeira !
development and investment if given the political and
social licence to expand and develop, with public awareness/
acceptance of its role. As all our AE event, AE2021 will feature a special
international trade exhibition, where Portuguese and
AE2021 will take place from October 4-7, 2021 in Funchal, international companies will present their latest products
Madeira. Madeira is part of the archipelago with the same and services. Standard and Corner booths are available and
name, one of the Autonomous Regions of Portugal, and each booth is 6m2 (2x3m) and features walls, carpet, two
situated about 1,000 km south of Lisbon and 650 km east of chairs and one table, spotlights, one power outlet, fascia
the African coast. Madeira is also part of the Macaronesia identification sign and two free full delegate registrations
ecoregion composed of the Azores, the Republic of Cape for the conference. Additional staff can register through the
Verde and the Canary Islands. booth contract at significantly reduced rates.
The conference plenary and parallel sessions will address the AE 2021 will also feature an Industry Forum, where
overall topic and abstract submission will be available within presentations and panel discussions focus on relevant
the coming weeks at the AE2021 web site. We are currently and timely issues for the sector and our AE Innova-
working hard with our local organising committees, headed tion Forum looking to help accelerate new companies.
by Carlos Andrade (ARDITI, CIIMAR-University of Porto,
The EAS thematic groups also organise special sessions
Portugal) and Luís Conceição (Sparos, Portugal) to prepare
this event and the AE2021 Programme Co-chairs Maria
and/or workshops within AE2021 and there will be
Teresa Dinis (CCMAR-University of Algarve) and Sachi satellite workshops of EU projects and other events
Kaushik (INRAE and EAS Past President) are finalising the taking place around the trade exhibition. Technical and
list of sessions for abstract submission. touristic tours will also be organised.
Important dates: Contacts:
AE2020 Cork - April 12-15, 2021
General conference and EAS
Abstract deadline: December 31
membership: eas@aquaeas.eu
Early Bird registration deadline: February 15
Booth sales, exhibitor contracts,
AE2021 Madeira - October 4-7, 2021
sponsorship and media partners
Abstract deadline: May 1
mario@marevent.com
Early Bird registration deadline: July 15
Aquaculture Europe • Vol. 45(2) September 2020
8
ARTIC LE
The prospect of phage
therapy in fish hatcheries
Bacteria and aquaculture
Aquaculture hatcheries are environments of high complexity, where the
developing larvae are in a delicate equilibrium with many different organisms,
including bacteria, microalgae and live preys, such as rotifers and copepods
provided by the fish farmers at the early developmental stages of fish. The role of
microbiota at these stages is crucial and only recently have we begun to understand
its significance. The establishment of a healthy microbiome in the developing
larvae is not only important for their survival but also for their future development
and performance during grow out. Environmental and food-borne bacteria
shape the gut microbiome of the developing larvae which will be later involved
in digestion, immune system development and subsequently growth and survival.
Recent studies have indicated vast differences between the various culture systems
(e.g. RAS vs flow-through) but also between individual larvae of the same tank
(for a review see Vadstein et al 2018). However, it is largely accepted that fast-
growing opportunistic bacteria pose the most significant threat in these systems.
Vibrio is likely the most significant genus of opportunistic bacteria associated with
disease outbreaks not only in marine fish but also in other farmed aquatic animals,
including crustaceans and bivalves.
Recent advancements in genomic sequencing technology have revealed a very big
diversity of Vibrio species that were previously misidentified or overlooked because
of the resolution limitations of biochemical tests commonly used at the diagnostic
labs. In the past, Vibrio anguillarum was acknowledged as the most devastating
member of the Vibrio genus. Now, we know that several other species can be at
least equally or even more virulent than V. anguillarum such as V. harveyi and V.
alginolyticus. Other species considered as bivalve pathogens are now increasingly
implicated in morbidity and mortality of fish larvae like V. tubiashii and V.
splendidus. And as we advance our analytical capabilities it is certain that more
species will be added in the pathogenic/opportunistic members of the Vibrio genus.
Controlling bacterial populations in the hatchery environment has for long been
recognized as critical for sustaining good health and development of fish larvae.
Many tools have been or are being used towards this direction. Water treatment
PAN T E L I S K AT H A R I OS through mechanical or UV and ozone filtration, is by far the most commonly
I N ST I T U T E O F M A R I NE B I OLOGY,
employed in aquaculture. In addition to water treatment, many hatcheries
BI OT E C H N O LO GY A ND “disinfect” live feeds before administration to fish larvae. Water treatment and
AQ UA CU LT U R E, H E LLENI C disinfection may seem rational, however this process destabilizes the microbial
C E N T R E FO R M A R I N E R ESEA R CH , ecology of the aquaculture systems, providing niche to fast-growing opportunistic
HERA K L I O N 7 1 5 0 0 , C R ETE, GR EECE bacteria to recolonize the available surfaces (from fish mucosa to physical
AQ UAT IC B I O LO G I CA LS substrates of the tanks). Another widely studied tool is the probiotics, beneficial
(WW W. A Q UAT IC- B IOLOG I CA LS.COM ) bacteria that colonize the fish gut and compete pathogenic microbes. Probiotics
E M A I L : KAT H A R I OS @ H CM R .GR have good potential, however research towards the sustained and prolonged
colonization of the fish gut and towards the use of aquatic vs terrestrial probiotic
strains is still needed for improving their efficacy. Prebiotics which are non-
digestible feed ingredients that selectively promote growth of beneficial bacteria in
the gut have also gained attention of the aquaculture industry. Lately, synbiotics
(combination of pro- and prebiotics) have also been considered as a means of
controlling bacteria in the hatchery environment.
All these tools however have one common denominator; they are not specific or
targeted. In an ideal situation, an intervention for controlling bacteria should be
targeted exclusively to the unwanted or pathogenic bacteria, leaving the beneficial ones
unaffected. Phage therapy is such a tool.
continued on page 10
Aquaculture Europe • Vol. 45(2) September 2020
9
ARTI C LE
1. A. Schematic representation of the structure of a Myoviridae bacteriophage (by Chelsea Bonnain, Mya Breitbart and Kristen N. Buck
licensed under CC BY-SA 4.0). B. Transmission Electron Microscopy image of a Myoviridae bacteriophage showing the contractile tail
(courtesy of Dr. Pantelis Katharios)
Bacteriophages and phage therapy host cell, a lytic phage will start producing its structural
proteins and genetic material which will be self-assembled
Bacteriophages or phages are viruses that exclusively infect and packaged inside the host cell making up the progeny
bacteria. They are the most abundant life entity1 in the virions. After the completion of this process, the newly
planet. Their number is astronomical; it has been estimated assembled phages will secrete lytic enzymes that will degrade
that there are approximately 1031 phages in the biosphere. the bacterial cell wall from the inside resulting in a burst
Phages were discovered more than 100 years ago; initially that will release them to the external milieu. The number of
Ernest Hanbury Hankin, an English microbiologist working new virions produced in a single bacterial host cell is called
in India made the first hypothesis of their existence before the burst size and can vary significantly between different
the end of the 19th century. In 1915, another English phages but also between different types of infections. The
microbiologist, Frederick William Twort published the other type of phage is the temperate one. After infection,
first scientific paper in the journal Lancet, describing the DNA of this phage is inserted inside the chromosome
the activity of bacteriophages. But it is Felix d’ Herelle, of the bacterial hosts. Once the viral DNA is integrated in
a French microbiologist of the Pasteur Institute who is the bacterial one, the phage (now called prophage) becomes
considered by many the discoverer (and also the name-giver) “dormant” and replicates along with the bacterium until it is
of bacteriophages. D’ Herelle published a paper in 1917 induced by either a DNA damage of the host or following
describing bacteriophages as viruses parasitic on bacteria. an environmental cue. When the prophage is induced, its
DNA is excised from the host’s DNA and the phage follows
Before we examine the potential of phage therapy in aquaculture, the lytic cycle which was described previously to release the
we need to discuss some basic notions of phage microbiology. new virions (Figure 3). During the prophage stage (when
Bacteriophages are the most efficient “predators” of bacteria a temperate phage is integrated in the bacterial host), its
in nature. Their ecological significance is huge as they control genes may become functional genes of that host. Therefore,
the number of bacteria in the environment. The structure the infected bacterium which is called a lysogen may carry
of phages (Figure 1) comprises a proteinaceous capsid that and express new traits that originally belonged to the phage.
encapsulates their genetic material (DNA or RNA) and The problem arises when such phage genes encode toxins
in many cases a tail which is attached to the capsid. There and proteins implicated in antibiotic resistance. It is known
are many different morphologies of bacteriophages, tailed that transduction is one of the most commonly observed
and non-tailed, but here we will mostly focus on tailed ways of gene-transfer in bacteria and it is facilitated by the
bacteriophages. Bacteriophages’ tails can be long or short, temperate bacteriophages. Such an example is the cholera
contractile and non-contractile and this character is also used toxin, which is the main virulence factor of Vibrio cholerae,
for taxonomical purposes. At the end of the tail there is the encoded in a prophage integrated in the chromosome of
baseplate on which there are the tail fibers and the spike. the bacterium. Likewise, marine pathogenic vibrios like V.
At the distal end of the tail fibers there are receptor binding harveyi, V. alginolyticus, V. vulnificus and many others carry
proteins which interact with specific surface receptors of the prophage-encoded toxins which make them more virulent
bacterial host. Spike proteins display enzymatic activity which than the non-phage-infected ones. This process of acquiring
is used for the degradation of the lipopolysaccharide layer new properties that may increase the bacterial fitness or more
of bacterial surface to facilitate binding of the phage to the importantly their virulence is called lysogenic conversion.
bacterial receptors. Once the phage is irreversibly attached to And it is exactly this feature that creates the biggest
the bacterial surface it will inject its genetic material inside risk in using phages as a therapeutic tool: the accidental
the cell (Figure 2). From this moment on, the phage, as all transformation of non-virulent bacterial strains to virulent.
viruses do, will hijack the bacterial cell machinery for its It is of the greatest importance therefore to select only lytic
own purpose which is propagation. There are at least four phages and discard the temperate ones in phage therapy.
different types of phages according to their life cycle. The Moreover, nowadays a more precise selection of appropriate
two most well-known and studied are the lytic or virulent phages is based on genomic analysis. Following whole
and the temperate. Following its DNA injection to the genome sequencing we can now screen the genomic arsenal
1
there is an ongoing scientific debate whether viruses are nonliving or living organisms, see: https://www.scientificamerican.com/article/are-viruses-alive-2004/
Aquaculture Europe • Vol. 45(2) September 2020
10ARTIC LE
bacterial cell. But even after the penetration of the bacterial
wall, the bacterium has mechanisms that confer resistance
against phage infection. The CRISPR-Cas system is actually
a bacterial “adaptive immune system” against phages. On
the other side, phages also very rapidly adapt and develop
counter-resistance measures. Since the ability of bacteria to
develop resistance against phage infection is often related to a
downregulation of receptors which are being used for nutrient
acquisition or by modification of the LPS which is a virulence
determinant, in many cases, resistant strains are less fit or less
virulent than the wild type3. Therefore, the development of
resistance has a significant cost for the bacteria. The rapid
development of bacterial resistance against phages is one
of the main drawbacks in phage therapy. This resistance
development is almost certain to happen over a period of
time. To overcome this problem, phage therapy should be
carefully designed. Combination of different phages termed
as “phage cocktails” is the solution. However, the use of the
2. Schematic representation of phage attachment to the bacterial
correct ingredients for these cocktails requires expertise and
cell and injection of its nucleic acid (licensed under CC) knowledge. In the past, phage cocktails were created with
phages displaying different host ranges. Now, we know that
a successful phage cocktail should ideally contain phages
of phages to discard those who have “suspicious” or unwanted that use different receptors for the initial attachment to the
genes. Temperate phages for example carry “signature” genes bacterial host. This is because development of resistance
like integrases required for the successful integration of their from the bacteria is costly, and changes (like downregulation
DNA into the host’s DNA. Modern bioinformatics tools can or mutations) in more than one or two receptors might
easily detect this type of genes if the genome of a phage is jeopardize their viability. Lately, phages with very large
available. genomes termed as “jumbo” phages have demonstrated wide
host range which is probably related to a wider diversity of
Phages are usually highly host specific. Sometimes their
receptor binding proteins in their tails. These phages are also
host specificity is down to the strain level. However, there
very promising ingredients of phage cocktails.
are also phages with a broad host range2 spanning most
commonly different species of the same genus. This feature Phage therapy trials in aquaculture
differentiates phage therapy from all other tools we currently
have for controlling bacteria in aquaculture. Phage therapy is The initial attempt to use phages against fish pathogenic
a targeted and precise treatment. Host specificity of phages bacteria goes back to the 80s. The first scientific report was
depends on complex molecular interactions between the from Taiwan and was published in Fish Pathology in 19814
phage and the bacterium throughout the infection cycle, and regards phage therapy against Aeromonas hydrophila
which is outside the scope of this article. However, one of the infection of loach. Since then, many scientific papers from
most important factors is the type and diversity of receptor various countries describe phages with therapeutic potential
binding proteins found on the phage tail, which will be or use phages as a means of therapy in aquaculture. The
used for the first interaction between phage and bacteria. In majority of the first research trials focused on the use of
Gram-negative bacteria like vibrios, the main target of these phages as a method to treat infected fish and the results
phage proteins are the components of their outer membrane were variable. In the challenge tests which have been used to
like the lipopolysaccarides (LPS) which are major virulence assess the efficacy of phage therapy, phages are commonly
factors, the flagella, and the porins which are receptors used administered simultaneously with the infectious agent.
by the bacteria to obtain nutrients from the extracellular This results in a significant decrease of the number of the
milieu. bacteria available for initiating the infection and subsequently
in positive results. However, there are very few properly
Phages and bacteria are in a constant arms race in the designed studies which would be useful to explore the true
environment. Bacteria are continuously exposed to phage efficacy of phages as therapeutics. Ideally, these should use
“predation” and in order to survive they must devise strategies a variety of pathogenic strains of the bacterial target and a
to resist phage infection. Bacterial resistance against phage phage cocktail that would be administered after the onset of
infection may develop very fast. Usually, bacteria will sacrifice the infection.
the receptors to which phages are attached. This is controlled
at a molecular level and involves the downregulation of The administration of the phages in aquaculture is usually
the genes which encode for the proteins of these receptors. done either directly in the water or in feed. Coating of phages
Resistance can also be developed through genetic mutations in feed pellets has been proven effective in studies conducted
of these proteins that will result in compatibility loss of the with rainbow trout as the phages could be detected in various
phage binding receptors proteins and the receptors of the organs of the experimental fish after feeding, showing the
ability of the phages to survive passage through the fish
stomach. Of course, there are several things that should be
2
Host range: The taxonomic diversity of hosts a phage can infect
considered when designing a proper therapeutic scheme. The
3
a strain which prevails among individuals in natural conditions, as distinct from an atypical first is the target bacterial pathogen and the diversity of its
mutant type strains. Then it is the dose, which is called Multiplicity of
4
Wu, J.L., Lin, H.M., Jan, L., Hsu, Y.L. and CHANG, L.H., 1981. Biological control of fish Infection (M.O.I.) in phage microbiology and it is the ratio
bacterial pathogen, Aeromonas hydrophila, by bacteriophage AH 1. Fish Pathology,
15(3-4), pp.271-276 continued on page 12
Aquaculture Europe • Vol. 45(2) September 2020
11ARTI C LE
3. The lytic and lysogenic life cycle of phages. Lytic or virulent bacteriophages follow exclusively the lytic cycle, whereas temperate
bacteriophages follow the lysogenic cycle and are integrated in the bacterial chromosome as prophages. Once induced they will be
excised from the bacterial chromosome and will follow the lytic cycle. The diagram is a modification of a diagram licensed under CC.
of phage particles to bacteria. This is determined in the lab that biofilm might enhance their survival. This is a very
during the characterization of the phage. A high M.O.I. important finding since it suggests that phages can survive
suggests that a large number of phages should be used for the water treatment processes of RAS and can be used
treatment which of course is directly related to an increased prophylactically in those systems to control unwanted
production cost. Another important parameter is the location pathogenic bacteria in a targeted way.
of the target pathogen (water, mucosa, internal organs,
intracellular, etc.). However, it is the use of phages as a means of controlling
bacteria in the hatcheries that has the greatest potential.
Phage therapy is very attractive for aquaculture. Even though modern marine hatcheries are areas of increased
Bacteriophages are ubiquitous in the aquatic environment. biosecurity, pathogenic bacteria continue to find their way
The aqueous nature of the water facilitates their diffusion into the fish rearing tanks causing morbidity, mortality,
and increases the likelihood of colliding to the target bacteria. and inconsistency in the production performance. The
Moreover, phages in the water can pass through the gills administration of live feeds is the vehicle for their entrance.
and stomach (marine fish drink water) into the blood flow As stated at the beginning of this article, the disinfection
and may reach the internal organs. Since phages are natural of the live feeds will have an impact on the much-needed
inhabitants of the aquatic environment, their medicinal healthy colonization of the fish gut by beneficial bacteria.
use could be compatible with organic farming. Phage will A recent use of phages proposed by our group is the use
not leave residues as it is in the case of antibiotics and are of phages as a “smart disinfectant” of live feeds. We have
completely harmless to fish, humans, and the environment. developed and used wide host range phage cocktails that can
Phages are viruses which are self-replicating agents and in selectively reduce vibrios in the live feeds. We have shown
theory, phage therapy would not require multiple dosing. that following a single administration of vibriophages during
Moreover, the high host specificity of phages makes the enrichment process of live Artemia for four hours, a
them the ideal solution of controlling bacteria in sensitive reduction of 93% was observed in the vibrio load of the
environments like the fish hatcheries and the RAS. Finally, treated group vs the untreated one. We are developing phage-
phages can be used at the early developmental stages of fish based disinfectants against vibrios of the Harveyi clade like V.
where vaccination cannot be applied because the immune harveyi, V. owensii, V. alginolyticus etc. which include serious
system is not mature. opportunists commonly found in live feeds. These pathogens
are linked to the larval enteritis of gilthead seabream which
In a recently published research conducted in Finland5, results in mass losses in many Mediterranean hatcheries. One
phages of Flavobacterium persisted for 14 days in the tanks of the benefits of this method is that the treatment is done in
of a RAS following single administration. Moreover, the the batch cultures of live feeds, thus significantly reducing the
persistence of phages was longer in the biofilters suggesting
5
Almeida, G.M., Mäkelä, K., Laanto, E., Pulkkinen, J., Vielma, J. and Sundberg, L.R., 2019. The fate of bacteriophages in recirculating aquaculture systems (RAS)—towards developing
phage therapy for RAS. Antibiotics, 8(4), p.192.https://www.mdpi.com/2079-6382/8/4/192
Aquaculture Europe • Vol. 45(2) September 2020
12ARTIC LE
chances of bacteria to develop resistance against the phages. that significantly differentiates their licensing process from
Such innovative products as the phage “smart disinfectant” the accepted norm. More importantly, the ingredients of a
are developed by Aquatic Biologicals6, a spin-off company of phage therapy product should be revised and replaced often
the Hellenic Centre for Marine Research which was recently to overcome resistance issues. Since every single element of
established to develop innovative aquaculture health products. a pharmaceutical product should be extensively tested for
safety and efficacy before allowing it as a new component
Similar actions have been documented for salmon hatcheries of a licensed product, it is more than evident that licensing
where bacteriophages have already been used as a biocontrol of phages will be impossible for the pharma industry.
agent for Yersinia ruckeri. This pathogen is responsible for Furthermore, the production of phages as pharmaceuticals
Enteric Red Mouth disease or Yersiniosis. A Norwegian at GMP (Good Manufacturing Practices) level is more
company, ACD Pharmaceuticals has developed and licensed than challenging and of course extremely costly. There is a
for Norway a commercial phage product that could be used strong lobby pushing the regulatory authorities for adjusting
prophylactically to control Yersinia in salmon tanks. the legislation in a way that phage therapy will become an
economically feasible and safe option especially in the era
Challenges of phage therapy
of antimicrobial resistance where alternatives are urgently
Although it is more than a century of phage research, phage needed.
therapy faces significant challenges before it is widely adopted
On the other hand, licensing phage products not as
as a treatment/prevention method at an industrial scale.
pharmaceuticals but rather as biocontrol agents or water
Culot, Grosset and Gautier, researchers of INRA, France,
quality enhancers might be a more viable solution for the
have recently provided an excellent review of the challenges of
time being. Companies like ACD Pharmaceuticals have
phage therapy for commercial aquaculture7.
already followed this path and a commercial product based on
The results of phage therapy are still inconsistent. This is phages under the trade name CUSTUS is already available in
mainly due to the improper design of the phage therapy Norway as a biocontrol agent of Yersiniosis in salmon.
products and application schemes. An extremely important
prerequisite for efficacious and safe phage therapy is the
Acknowledgements
thorough characterization of the phages. The elements of Dr. Katharios has received funding to develop innovative
phage microbiology which were presented previously in this phage therapy methods for marine fish hatcheries by the OP
article need to be studied at the laboratory very carefully. Fisheries and Maritime 2014-2020 Innovative measures,
Knowledge of the burst size, the host range, the life cycle and Innovation 2019 co-funded by Greek and EU funds.
the genetics of any candidate phage will dictate not only how
suitable the phage is as a therapeutic agent but also the best Further reading
way of its application (how much to give, when, etc.)
Readers seeking more information on the topics developed
A very big challenge is to overcome the resistance in this article may refer to the selected literature below (open
development from the side of bacteria. As explained in this access articles freely accessible for the public):
article, resistance development is the outcome of coevolution
of phages and bacteria and it is a natural phenomenon. Phage Vadstein, O., Attramadal, K.J., Bakke, I., Forberg, T.,
cocktails will provide the solution, however the formation Olsen, Y., Verdegem, M., Giatsis, C., Skjermo, J., Aasen,
of potent cocktails is still challenging and requires advanced I.M., Gatesoupe, F.J. and Dierckens, K., 2018. Managing
knowledge and analytical skills. the microbial community of marine fish larvae: a holistic
perspective for larviculture. Frontiers in microbiology, 9,
Mass production of phages is also a very big challenge for the p.1820.
pharma industry. Production of phages in bioreactors is not
an easily standardized process. Moreover, in the case where Kalatzis, P.G., Castillo, D., Katharios, P. and Middelboe,
phages are to be used as a therapeutic agent, specific quality M., 2018. Bacteriophage interactions with marine pathogenic
standards should be met, like the absence of endotoxins vibrios: implications for phage therapy. Antibiotics, 7(1),
which are released after the lysis of the Gram-negative p.15.
bacterial hosts. Although this is technically feasible, it
Kalatzis, P.G., Bastias, R., Kokkari, C. and Katharios,
significantly increases the production cost.
P., 2016. Isolation and characterization of two lytic
The biggest challenge, however, is the regulatory barriers bacteriophages, φSt2 and φGrn1; phage therapy application
found in many countries including the EU and USA. for biological control of Vibrio alginolyticus in aquaculture
Licensing of phage products as pharmaceuticals is a live feeds. PloS one, 11(3), p.e0151101.
nightmare. Phages are unconventional pharmaceuticals, a fact
6
www.aquatic-biologicals.com
7
Culot, A., Grosset, N. and Gautier, M., 2019. Overcoming the challenges of phage therapy for industrial aquaculture: A review. Aquaculture, 513, p.734423.
Aquaculture Europe • Vol. 45(2) September 2020
13ARTI C LE
Figure 1- Biofloc Fish Farming tank.
Biofloc Based Fish the filamentous microorganism, or held
together by electrostatic attraction. The
biofloc community also includes animals
Farming (BFT): that are grazers of floc, such as some
zooplankton and nematodes. Large
biofloc can be seen with the naked eye,
but most are microscopic.
A New Approach For The nutritional quality of biofloc to
Employment Generation & the cultured animal is good but rather
variable.
Sustainable Aquaulture in India The dry-weight protein content of
biofloc ranges from 25 to 50 per cent,
with most estimates between 30 and 45
Aquaculture production depends on feed, percent. Fat content ranges from 0.5 to
M R DE BTA N U BA R MA N, dissolved oxygen and maintenance of 1.5 per cent, with most estimates between
A Q UA CO N S ULTA NT,
FO U N D E R & CEO, A QUA D OCTOR
water quality parameters in an optimal 1 and 5 percent. There are conflicting
S O LU T IO N S, KOLKATA , range. There are strong economic reports about the adequacy of biofloc to
W EST B EN G AL, I ND I A incentives for aquaculture businesses to provide the often limiting amino acids
EM A IL : D E BTA NU0 80@G M A I L.COM be more efficient with production inputs, methionine and lysine. Biofloc is a good
especially feed and those required for source of vitamins and minerals, especially
managing feed-induced water quality phosphorus. The core advantage in biofloc
issues. High-density rearing of fish systems is whatever the waste around
typically requires some waste treatment from feed or faecal matter from fish
infrastructure. Bio-floc systems use a which accounts for about 70% of the total
counter-intuitive approach to allow energy given in feed, goes to the system
or encourage solids and the associated as the waste. Thus at intensive culture
microbial community to accumulate in operation maintaining water quality
the water. As long as there is sufficient becomes a challenge. So reusing the
mixing and aeration to maintain an active lost nutrients through floc development
floc in suspension, water quality can be becomes a wise way for increasing feed
controlled in a better way. Managing efficiency and the maintaining water
biofloc systems is not as straight forward quality.
as that, however, and some degree of
technical sophistication is required for the Dried biofloc has been proposed as an
system to be fully functional and the most ingredient to replace fishmeal or soybean
productive. meal in aquafeeds. Its nutritional quality
is good, and trials with shrimps fed
Biofloc is a collection (flocs) of algae, diets containing up to 30 percent dried
bacteria, protozoans and other kinds biofloc show promise. Nonetheless, it is
of particulate organic matter such as unlikely that dried biofloc could replace
faeces and uneaten feed. Each floc is the animal or plant protein sources
held together in a loose matrix of mucus used in commercial-scale aqua feed
that is secreted by bacteria, bound by manufacturing because only limited
Aquaculture Europe • Vol. 45(2) September 2020
14ARTIC LE
quantities are available. Furthermore, the cost-effectiveness of
producing and drying biofloc solids at commercial scale has to
be demonstrated.
Floc stimulate immune response in fish. Its is well established
that the immune response of animal reared in the biofloc
based systems is better than the other control culture. A
possible reason is the presence of bacteria and other microbial
assemblages give specific nutraceutical and immunogenic
effects.
Heterotrophic bacteria (Bacillus subtilis, Bacillus licgenuformis,
Bacillus coagulus, with a mix of Nitrobacter and Nitrosomonas)
are required for initial floc growth, then assemblage of algae,
green algae, diatoms, zooplankton including rotifer nematodes
copepods etc also required for floc growth. In greenwater
systems, biofloc algae dominate and in brown water biofloc Figure 2. Harvested Vietnam Koi (Anabas sps.)
bacteria dominates. Floc species show natural growth and
succession so the floc quality and water colour is monitored
and managed regularly.
Biofloc Systems and species
Biofloc technique is waste treatment method. Biofloc
provides two critical services—training waste from feeding
providing nutrition to the fish from floc consumption. Biofloc
systems can operate with low water exchange rates (0.5 to 1
percent per day). This long water residence time allows the
development of a dense and active biofloc community to
enhance the treatment of waste organic matter and nutrients.
In biofloc systems, using water exchanges to manage water
quality is minimized and internal waste treatment processes
are emphasized and encouraged. The potential benefit of
biofloc systems is the capacity to recycle waste nutrients
through microbial protein into fish or shrimp. About 20 to 30
percent of the nitrogen in added feed is assimilated by fish,
implying that 70 to 80 percent of nitrogen added as feed is
released to be to the culture environment as waste. In biofloc
systems, some of this nitrogen is incorporated into bacterial
cells that are main components of biofloc. Consumption of
this microbial protein, in effect for a second time, contributes
to growth.
The biofloc system is benifecial for the species that to be
cultured that are able derive some nutritional benefit from
the direct consumption of floc. Biofloc systems are also most
suitable for species that can tolerate high solids concentration
in water and are generally tolerant of poor water quality such
as Tilapia, Pangassius, Anabas, Magur, Singhi and Common
carp etc. Some of them like Tilapia, Common carp and
Shrimps have physiological adaptations that allow them to
consume biofloc and digest microbial protein, thereby taking
advantage of biofloc as a food resource. Figure 3 : Greenwater Biofloc System
Only a relatively few types of biofloc systems are used in
commercial aquaculture or have been evaluated in detail in
research. The two basic types are those that are exposed to
natural light and those that are not. Biofloc systems exposed
to natural light include outdoor, lined ponds for shrimp & fish
culture in greenhouses.
A complex mixture of algal and bacterial processes control
water quality in such “Green Water” biofloc systems (Fig:-3).
Most biofloc systems in commercial use are green water.
However, some biofloc systems (raceways and tanks) have been
installed in a closed building with no exposure to natural light.
These systems are operated as “Brown-Water” biofloc systems Figure 4: Brownwater Biofloc System
(Fig-4), where only bacterial processes control water quality.
continued on page 16
Aquaculture Europe • Vol. 45(2) September 2020
15ARTI C LE
Maintaining active bioflocs A suspended solids concentration of 200 to 500mg/L is
sufficient for good system functionality and will control
Intensive turbulent mixing is an essential requirement of ammonia without excessive water respiration. The best
biofloc systems. Solids must be suspended in the water increase in suspended solids concentration (250 to 500 mg/L)
column at all times or the system will not function. Without and the associated rapid increase in water respiration (6mg
mixing, biofloc settle out of suspension and may form piles O2/L per hour). This requires a five-fold increase in aerator
that rapidly consume nearby dissolve oxygen. These anaerobic power from 30to 150hp/ha to match the oxygen demand.
zones can lead to the release of hydrogen sulphide, methane Most of this increasing energy demand is required to
and ammonia that are highly toxic to shrimp and fish. Solids maintain biofloc in suspension.
can be removed by periodic flushing or by pumping sludge
from the pond centre. In intensive, green water raceways Dynamics of Ammonia
for shrimp, water respiration rates range from 2 to 2.5mg
O2/L per hour, although it can be as high as 6 mg O2/L A major goal of water quality management in any aquatic
per hour. It is absolutely essential to providing sufficient animal production system is maintaining ammonia
aeration or oxygenation to meet this high oxygen demand concentration below toxic levels. In Biofloc systems, there
and to maintain concentration at safe levels. These high are three main processes that control ammonia, algal uptake,
respiration rates also indicate that the response time in the bacterial assimilation and nitrification. The transformations
event of a system failure is very short, often less than 1 hour. and dynamics of ammonia in biofloc system are complex,
Thus monitoring, alarms, and emergency power systems are involving interplay among the algae and bacteria that
required elements of biofloc systems. compete for ammonia. The relative importance of each
process depends on many factors, among them the daily
Floc develops gradually in this system and first, the system feeding rat, suspended solids (biofloc) concentration,
will abruptly transition from green water, an algal system ammonia concentration, light intensity, and input carbon-to-
to brown water, bacterial system. As daily feeding rate nitrogen (C:N) ratio.
increases from 100 to 200kg/ha (10 to 20g/m2), the water
will appear green with the dense algae blooms. Algal uptake In Biofloc system, a major factor that controls ammonia con-
is the main mechanism for ammonia control. The aerator centration is the C:N ratio. A feed with 30 to 35 per cent pro-
power required at this feeding rate is about 25 to 30hp/ha. tein concentration has a relatively low C: N ratio, about 9 to
At a daily feeding rate of 300 kg/ha, there is an abrupt shift 10:1. Increasing the C:N ratio of inputs to 12 to 15:1 favours
when the lack of light at very high algal density hinders the heterotrophic pathway for ammonia control. The low C:N
photosynthesis. Bacteria begin to grow and biofloc develops, ratio of feed can be augmented by adding supplement materi-
as indicated by feed consumption in shrimp raceway biofloc als with a high C: N ratio. Or the inputs C: N ratio can be
systems at an e solids concentration of 100 to 300mg/L. increased by reducing feed protein content. Ammonia Control
Imhoff or setting cones are a simple way to index suspended through the heterotrophic pathway is often, more stable and
solid concentration. The cones have marked graduation reliable than algal uptake or nitrification.
on the outside that can be used to measure the volume of
solid that settles from 1 liter of system water. The interval of For every 1kg of 30 to 38 per cent protein feed added add 0.5
time should be standardized and convenient, usually 10 to to 1kg of a carbohydrate source such as sugar. It is clear that
20 minutes. Solids also can be measured with a TDS meter. relatively large quantities of carbohydrate must be added to
Maintaining a settleable solids concentration of 15 to 30ml/L control ammonia concentration this way.
will provide good functionality in biofloc systems.
Bacterial Assimilation, nitrification and
Alkalinity is the capacity of water to buffer or resist changes algal uptake
in pH in response to additions of acids or base. Water in
biofloc systems should be maintained with sample reserve Many of the early names for biofloc systems included the
of alkalinity because it is constantly depleted by reaction word “ heterotrophic”, which describes a group of bacteria
with acid added to water. The activity of nitrifying bacteria is that, by definition, obtains carbon from organic sources.
responsible for most losses of alkalinity in intensive biofloc Despite large inputs of feed to intensive systems, the growth
systems. Over time, acid produced by nitrification wears of heterotrophic bacteria in biofloc systems is limited by
down the reserve of alkalinity in the water. Once alkalinity is dissolved organic carbon. To stimulate the production of
depleted, pH can drop steeply, inhibiting bacterial function, heterotrophic bacteria, the C:N ratio of inputs is raised by
including that of the important nitrifying bacteria. adding a supplement source of carbohydrate or reducing feed
protein level. By this manipulation, heterotrophic bacteria
Alkalinity can be recovered in denitrification units. Nitrate
create a demand for nitrogen(as ammonia) because organic
accumulates in most intensive biofloc systems because of
carbon and inorganic nitrogen are generally taken up in a
ongoing nitrification. If unchecked, nitrate concentration
fixed ratio that reflects the composition and requirement of
reflects the cumulative feed loading to the system. Nitrate
bacterial cells. Thus ammonia can be controlled by adding
accumulation can be tempered by partial dilution through
organic carbon to stimulate the growth of heterotrophic
water exchange.
bacteria.
Solids Management and sludge treatment Similar to algae, ammonia is “immobilized” while packaged
In biofloc systems, waste solids are allowed to accumulate in heterotrophic bacterial cells as protein. Because the growth
and additional solids are encouraged by intensive aeration rate of heterotrophic bacteria is so much greater than that of
and carbohydrate additions. Over time, and with sufficient nitrifying bacteria, ammonia control through immobilization
mixing, solids can be accumulated to undesirably high levels by heterotrophic bacteria occurs rapidly, usually within hours
(2,000 to 3,000 mg/L). Biofloc systems are typically operated or days if sufficient quality of simple organic carbon(e.g. sugar
at suspended solids concentrations less than 1,000mg/L and or starch)is added. The packaging of nitrogen in bacterial
the most often less than500 mg/L. cells is temporary because cell turns over rapidly and release
Aquaculture Europe • Vol. 45(2) September 2020
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