Publisher Version (Open Access)

Received: 15 June 2022 Revised: 22 December 2022 Accepted: 27 December 2022
DOI: 10.1111/raq.12784
REVIEW
Agricultural wastes for brine shrimp Artemia production: A

review
Nepheronia Jumalon Ogburn 1 | Luchun Duan 1,2 |

Suresh Ramraj Subashchandrabose 1,3 | Patrick Sorgeloos 4 | Wayne O'Connor 5 |
Mallavarapu Megharaj 1,2 | Ravi Naidu 1,2
1
Global Centre for Environmental
Remediation, The University of Newcastle, Abstract
Callaghan, New South Wales, Australia
An increasing global population has meant aquaculture, one of the fastest growing
2
Cooperative Research Centre for
Contamination Assessment and Remediation food industry sectors, faces significant sustainability challenges as it tries to address
of the Environment, Callaghan, New South the rising global protein demand. In many sectors, production is underpinned by
Wales, Australia
3
fishmeal as dietary ingredient, but this is a finite resource with competing users
Loam Bio, Orange, New South Wales,
Australia from the poultry and livestock industries. Alternatively, some (planktonic) aquatic
4
Laboratory of Aquaculture & Artemia species, especially brine shrimp Artemia, can be produced using agricultural waste
Reference Center, Ghent University, Ghent,
Belgium
to provide food or biomass to support increasing aquaculture demand. This review
5
New South Wales Department of Primary investigates research and production of Artemia using agricultural waste. Various
Industries, Port Stephens Fisheries Institute, systems used for Artemia production in inoculated ponds are analysed and dis-
Taylors Beach, New South Wales, Australia
cussed to provide options for environmentally sustainable food systems that can be
Correspondence applied from either an artisanal level in developing countries with a considerable
Nepheronia Jumalon Ogburn, Global Centre
for Environmental Remediation, The University labour force, or in intensive systems in countries with large volumes of under-
of Newcastle, Callaghan, NSW 2308, Australia. utilised resources, for example, sugar/alcohol-based waste and inland saline areas.
Email: [email protected]
Using agricultural waste, single cell protein production in a separate aerobic
Funding information digester can be a simple, continuous food source for Artemia to enable daily bio-
University of Newcastle and Cooperative
Research Centre for Contamination Assessment mass harvest. This could then be used as a fishmeal replacement or possibly for
and Remediation of the Environment human consumption to promote a circular economy by remediating waste to pro-
duce protein, like a food production mine.
KEYWORDS
aerobic digestion, Artemia production, circular economy, single cell protein, waste remediation
1 | I NT R O DUC T I O N: T HE I M P O R T A N CE
O F B R I N E SH R I M P P R O D U C T I O N A N D
UTILISATION IN AQUACULTURE
In recent decades, aquaculture has become the fastest growing major

Nepheronia Jumalon Ogburn should be first author.
food production sector globally, with production rising yearly at 7.5%
[The copyright line for this article was changed on 3 February 2023 after original online
publication] since 1970.1 At the same time, the proportion of wild fish stocks that
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited and is not used for commercial purposes.
© 2023 The Authors. Reviews in Aquaculture published by John Wiley & Sons Australia, Ltd.
Rev Aquac. 2023;15:1159–1178. wileyonlinelibrary.com/journal/raq 1159

17535131, 2023, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/raq.12784 by The University Of Newcastle, Wiley Online Library on [26/07/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
1160 OGBURN ET AL.
were being harvested within biologically sustainable levels decreased. 1. Investigate and summarise the use of agricultural wastes and by-
As the World's population approaches 10 billion, aquaculture is increas- products as a potential food source for Artemia farming.
2,3
ingly being called upon to fill the gap to feed growing populations. 2. Examine the direct application of agricultural waste as fertiliser in
While aquaculture plays a crucial role in global food security, it contrast to indirect use of waste in managed systems, like a flow-
also faces significant environmental challenges as production inten- through poultry/livestock and the biofloc system for Artemia
sifies. The reliance on fishmeal, fish oil and other products to feed fish production.
is potentially problematic because decreasing percentages of these 3. Compare the use of a separate aerobic digester system for Artemia
feed ingredients are processed from world fisheries production.1,4 The production with other waste-Artemia production systems and
poultry and livestock industries also compete for the use of these feed determine where each system is more suited; and
resources. Thus, there is a need to promote the increased use of alter- 4. Assess the potential of remediating high-volume waste, like
native protein sources in aquaculture5 and for industry and innovation vinasse or dunder from sugar-based alcohol distilleries, with
to scale healthy, sustainable feed alternatives.6 Australia as a case study, by utilising the waste as SCP food
Even if crop-based fishmeal replacement is found, the use of fish sources to produce nutritious Artemia.
oil will likely increase due to the absence of cost-effective alternative
lipid sources rich in long-chain polyunsaturated fatty acids (PUFAs),
especially to satisfy the requirements of higher trophic level finfish 3 | HI S T O RY OF P R O D U C T I O N O F T H E
and crustaceans. Production of marine microalgae or bacteria with B R I NE S HR I M P AR TEM IA U SI N G
high PUFA is currently too expensive for use in most aquaculture AGRICULTURAL WASTES
feeds, compounded by the problem of harvesting them in significant
volumes. The potential use of Artemia biomass grown using agricul- Since the early 1960s, when the importance of the brine shrimp, Arte-
tural waste as alternative food source and the different Artemia-waste mia, for aquaculture was first reported, there have been numerous
culture systems reported are investigated in this Review. overviews and documents on the biology, production and use of Arte-
Aquaculture development is constrained by the reliance on live mia.7,12,13 With the expansion of aquaculture and ensuing feed short-
7,8
feeds, which include the brine shrimp, Artemia. The demand for ages, increasing demand for this protein-rich shrimp with a
Artemia cysts continues to increase with the expansion of hatchery micrometre-thin shell has led to more studies on improved use, sourc-
production, and annual consumption is now estimated at 3500– ing of supplies, alternatives like microencapsulated diets, and growing
4000 tonnes to produce over 900 billion crustacean post-larvae and biomass indoors or in inoculated managed salt ponds.7
9
fish fry, with cysts sourced mostly from salt lakes and solar saltworks
with no to minimal management capabilities.
Artemia nauplii are the most common live feed used in larviculture 3.1 | Indoor production of Artemia using waste
of fish and crustaceans because they are easily cultured and are a suit-
able size for many larvae. Nauplii can be hatched overnight from easily Indoor high-density culturing of suitable algae as food for Artemia, is
transportable dry cysts (in contrast to most zooplankton used in aqua- mostly uneconomical or limited, so their use can only be considered
culture) and they have high nutritional value. Artemia is a continuous, in locations where algal production is an additional feature of the pri-
non-selective, particle-filtering organism, with 40%–67% protein mary aquaculture activity. The approach to on-growing batches of
according to life stages and feed. Artemia has a high reproductive Artemia to adults in indoor systems, using waste as a food source,
capacity, and a female can produce up to 300 nauplii or cysts every was pioneered in the Philippines when scientists from the Artemia
4 days, which can quickly grow to adults in 8–14 days, depending on Reference Center in Ghent, Belgium, introduced Artemia to the coun-
7
food and/or culture system. With its ability to grow well in extreme try and encouraged more research on its production and use. The
conditions, feeding on single cell protein (SCP) food,7,10 the potential problem of finding a cheap and suitable food for Artemia was over-
of Artemia biomass production to help address protein food shortage come by using rice bran as a cheap food source, and growing batches
and the dwindling fishmeal supply from marine sources should be fur- of Artemia adults in air-water-lift-operated recirculating raceways
ther explored, the more since current production is still very limited as (AWL).14 This was followed by studies using agricultural by-products
presented in this review. This can promote circular economies if, as and other feeds for Artemia to compare the quality of hatchery food
has been practised for millennia,11 waste can be used as a resource to for tiger prawns, Penaeus monodon,15 to lower the cost of using smal-
produce Artemia. This is becoming increasingly important for the ler Artemia nauplii from imported cysts or minimise reliance on micro-
future of aquaculture not only for profitability but also for sustainabil- algae that require huge cultivation space.
ity in an increasingly environmentally challenged industry. A study on the growth response of Artemia to various feeding
regimes, using Dunaliella tertiolecta as food,16 showed that Artemia lar-
vae are voracious feeders and one shrimp can clear 64 ml of water of
2 | AIMS 6,400,000 cells daily, and that over 10 million cells/shrimp/day can be
converted into faecal pellets by adult animals. This continuous filter-
With this review, we aim to: feeding capacity makes Artemia a great harvester for SCPs that mostly
OGBURN ET AL. 1161
T A B L E 1 Summary of publications on the use of agricultural waste for Artemia culture, emphasising biomass production and development of
indoor culture/tank production techniques.
Years Agricultural waste/by-product used Country Culture set-up/technique Products References

Indoor/tank culture
1980 Rice bran SEAFDEC, Iloilo, Fibreglass tanks (A-W-L Artemia biomass 18
Philippines operated raceways)
1982 Wheat flour, rice bran and milled SEAFDEC, Iloilo, Fibreglass tanks Milled rice and rice fed Artemia 22
rice-fed Artemia pre-adults Philippines juveniles gave better growth as
compared to mussel meat as feed for Penaeus monodon post-
prawn feed larvae)
1985 Rice bran (compared to microalgae, SEAFDEC, Iloilo, 2-L jars (1000 Artemia nauplii/L) Artemia (fed 3–5 days) as food for 15
corn, copra, and soybean diets) Philippines P. monodon post-larvae (PL 10)
Proved that Artemia quality (PUFA)
follows its diet and can be
manipulated
1987 Mono SCP yeast diet, and mixed Ghent, Belgium 300-L culture tanks in high- Artemia biomass—2-5 kg live 20
diets of yeast and micronised density (5000–15,000 Artemia weight per tank, after 14 days
corn-soybean, corn-wheat husks larvae/L) flow-through Mixed diets are suitable or better
and corn-yeast blended in brine recirculating system alternatives to rice bran
1987 Rice bran, microalgae from salt pan, India 2-L containers with 50 mg/L A mixed diet gave the best growth 23
soaked cabbage filtrate, salt pan seawater, stocked with 50 for parthenogenetic Tuticorin
Spirillum, yeast, and mix of all feed Artemia nauplii/L Artemia; maximum Artemia
length of 10.24 mm after
18 days
1987 Waste cabbage leaves, cow dung, India 159-L Cement tanks with a Best survival after 7 days obtained 24
poultry manure 10-cm sun-dried soil base with mixed waste compared to
individual waste
1987 Untreated rice bran blended in Mexico Four cement 1 cu m tanks, filled Artemia biomass growth similar up 25
seawater, chicken manure as with 375 L seawater, stocked to Day 10, better growth with
fertiliser for algae (vs. fresh with 1 Artemia nauplii/ml rice bran and Spirulina after,
Spirulina) then best with Spirulina from
Day 15.
1987 Dry, 44 μ-sieved defatted rice bran, United States Laboratory screw cap glass tubes Artemia biomass—Diets of rice 26
soybean, yeast lactoserum, (25 200 mm2), with 10-ml bran and Cerophyl most likely to
Cerophyl and Spirulina media and stocked 5 nauplii provide best results for large-
homogenised/diluted in seawater scale production under
condition of uncontrolled
bacterial contamination
1987 Rice bran, whey powder United States 430-L air-water-lift (AWL) Artemia biomass—rice bran shows 27
operated raceways better production of Artemia
adults; whey powder gave good
results for younger Artemia
1987 Dry, micronised feed (in water) of Portugal 2-L flask inoculated with 1 Artemia biomass—Ulva gave better 28
wheat bran versus Ulva nauplii/ml growth, survival, and food
(macroalgae) conversion efficiency than
wheat bran
1990–1992 Enzyme- and heat-treated and Belgium 21,29
chemically treated yeast—fresh
and dry
1992 Rice bran Philippines Semi flow-through Artemia Artemia biomass for feeding fish/ 19
culture unit shrimp
1994 Cow dung, pig dung, poultry manure India 10-L tubes, stocked with 100 Artemia biomass—better growth 30
and cabbage leaves in various nauplii/L using experimental diets than
combinations, with rice bran rice bran
suspension as control
1999 Micronised filtered rice bran and Australia 5-ton tanks operated as Air- Artemia biomass sold frozen, from 31
micronised wheat Water-Lift Raceway with an average yield of 12.3 kg/tank
filtration system, and partly for rice bran and 5.3 kg/tank for
introducing semi-flow-through wheat after 14–15 days of
culture
(Continues)
1162 OGBURN ET AL.
TABLE 1 (Continued)
Years Agricultural waste/by-product used Country Culture set-up/technique Products References

2000 Rice bran (control), black gram husk, India 200-ml glass containers stocked Artemia biomass—faster maturity 32
and red gram husk with 1000 nauplii/L with experimental diets than
with control
2008 Live and cooked cell wall deficient Belgium Sterile 500-ml glass bottles, each Four-day test to check yeast 33
Saccharomyces cerevisiae filled with 200-ml filtered effectiveness
autoclaved seawater and
stocked with 1000 germ-free
Artemia nauplii
2010 Wheat bran (with Dunaliella) Iran 1000-L AWL tanker in semi Artemia biomass (7116.7 g after 34
flow-through with 14 days)
2010–2011 Dunaliella salina biomass and water Australia Closed plastic-moulded (manhole Frozen biomass: although this is 35
(still containing high level of algae at the top) 32,000 L tanks reported as the first super-
cells) after the extraction of with a water inlet and filters intensive Artemia rearing system
carotenoids. that retain the Artemia in the in the World, there is no data
tank on the outlet, built near given on actual biomass
Dunaliella commercial ponds produced
2012 Wheat bran, soybean (each with Iran Glass bottles with 6-L saline Artemia biomass (4571 to 7018 g 36
Dunaliella) water with 6000 nauplii after 15 days)
2017 Molasses (compared to non-waste Bohai Bay, China 10-L plastic cones experiment Biofloc development for enhanced 37
sucrose, glucose, corn flour as Artemia production (14-day
carbon source) culture)
2018 Vermicompost manure leachate Sari, Iran 1-L cylindroconical glass tubes Possible to use VCL powder only 38
powder (VCL), originating from with 750-ml 33 mg/L water as much as 25% in the diet of
cow dung, with Dunaliella salina as Artemia; Best to grow Artemia
control, fed singly or in on algae for small laboratory
combination with algae cultures
Abbreviations: PUFA, polyunsaturated fatty acid; SCP, single cell protein.
require complex methods or costly equipment to harvest in significant like baker's yeast. However, they are included since yeast is sometimes
volumes because of their minute size. used as a reference diet,20 aside from being one of the earliest food
The use of SCP other than microalgae has been proven feasible tested for Artemia, or as a substitute for microalgae as live food.21
with trials of non-soluble by-products from agricultural crops or food-
processing, such as rice bran, corn bran, soybean pellets and lacto-
serum. These by-products have the advantage of being widely available 3.2 | Outdoor/pond production of Artemia using
and relatively inexpensive. They also provide ideal conditions for the waste
growth of suitable microflora, for example, Pseudomonas in rice bran,
which constitute an important food source in the diet of Artemia.17 Development of Artemia production using agricultural waste has pro-
Agricultural waste and by-products for Artemia indoor production gressed more significantly in outdoor systems and Artemia is now cul-
have been trailed mostly in small experiments and pilot tank trials to tured in countries where it is not endemic to address the expensive
reduce hatchery costs, but no large commercial indoor system has cost of importation and limited supply. There is also increasing inter-
been established. Batch production of Artemia in air-water-lift oper- est in ongrown Artemia, which had been much less frequently used in
ated raceways is not considered commercially attractive due to cost aquaculture hatcheries than nauplii. The preference for nauplii is due
18
and limited biomass output. However, improvement of static culture to their ease of production by simple overnight hatching of widely
systems has been reported using a simple semi flow-through Artemia available and storable cysts.
culture unit for possible integration in marine fish and shellfish hatch- Pioneering studies were reported in the Philippines to integrate
eries as the source of a cheap nursery diet and the possibility of pro- Artemia production in salt pond systems.39 This was followed by a much
ducing brine shrimp populations with a uniform size.19 larger development of an integrated system consisting of the first brack-
A summary of Artemia indoor production using agricultural wastes or ish water flow through salt-fish farm, poultry, and a cattle feedlot. This
by-products, collectively referred to in this review as ‘waste’, is provided development integrated a saline waste processing pond for Artemia bio-
in Table 1.The focus is on wastes from agricultural industries. Waste from mass and cyst production.10,40,41 This closed loop approach to farming,
manufacturing industries or domestic consumption is excluded. used agricultural wastes from one part of an agricultural landscape as
It should be noted that yeast reported as Artemia food in Table 1 is inputs to a subsequent phase, significantly increasing farm productivity
not necessarily sourced from industries that produce a significant amount and profitability while achieving reductions in greenhouse gas (GHG)
of spent yeast waste, but more commonly in more expensive pure forms emissions over traditional farming systems.41 This provided an
OGBURN ET AL. 1163
important social contribution through income-generating opportunities or undigested manure and could be used directly after a few days of
for poor rural communities. The estimated total cumulative annual GHG aeration. This study also showed that growth rates in treatments
emission savings from the integrated system amount to 12.9 tonnes where feed rate was based on cell volume calculations were signifi-
CO2-e per head of cattle passed through the feedlot for 300 days. The cantly better than those fed according to dry weight basis.
unitised ratios for the integrated system were: 1 ha sugarcane: 4 head The promising results obtained using vinasse to produce Artemia
of cattle: 0.13 ha saline waste processing pond that serviced both milk- biomass commercially suggest it would be beneficial to explore its
fish and Artemia ponds. application in Australia, where high volumes of waste are produced in
Culturing Artemia biomass requires considerable labour and infra- the sugarcane and sugar-based alcohol industries.
structure, unless the hatchery is situated near an Artemia commercial A summary of Artemia pond culture using agricultural wastes or
pond production system aimed primarily at biomass production. The by-products, is provided in Table 2. Design and operation details of
system in the Philippines was developed with this consideration to various systems can be found in the literature cited.
provide biomass for prawn hatchery or grow-out systems, and poultry Figure 1 illustrates the different aquaculture systems where Artemia
feed manufacture10,40 while relying on labour from marginal commu- has been grown and an overview of how agricultural wastes were used.
nities dependent on over-fished marine resource for their daily food.
The use of sugar-mill effluent as a food source for Artemia began
in the Philippines from 1988 to 1993, to increase Artemia biomass 3.3 | Benefits and prospects of indoor and outdoor
production further to feed Penaeid shrimps directly and later as part production of Artemia using waste
of the first documented integrated intensive grouper pond production
system supplying the local and export market.10,42 The integrated Depending on culture set-up, the use of Artemia biomass for feeding
grouper-Artemia farm provided alternative employment to 300 families hatchery post-larvae can result in improved economics, as expenses
in marginal communities to stop illegal fishing and encouraged them for cysts and weaning diets can be reduced. Artemia culture done as
to voluntarily engage in mangrove reforestation as soon as some fish- part of an integrated system produces a multiplier effect on profits,
ermen started earning a year's income within a week. while also reducing carbon footprint.
Sugar mill effluent was traditionally disposed of directly in rivers Large-scale production of good-quality Artemia biomass from agri-
or the sea, causing severe pollution and months of no catch for local cultural waste will benefit the aquaculture and aquarium industry as a
fishermen. However, high volume sugar mill waste, locally referred to live food source, a feed ingredient or fishmeal replacement, in shrimp/
as vinesse (or vinasse in other countries), increased cyst production to prawn broodstock maturation and hatchery production, in fish produc-
30 kg/ha/month and provided Artemia biomass standing crops of up tion, and even benefit other industries like poultry, which relies on fish-
to 10 tonnes/ha/day10 in a one-meter deep pond, enabling daily har- meal for feed production. It will also be a potential protein source for
vest (done on as needed basis only, so optimal daily harvest is not human consumption,27 as has been practised by some communities
determined but could feasibly go over 70 kg/ha/day) to feed shrimps where natural population of Artemia occurs. Furthermore, in Asia, Arte-
in the hatchery or to wean fish larvae. Commercial development in mia is now used as a major ingredient in Artemia omelette in Vietnam,63
the Philippines stopped in the1990s. or Artemia kebab in Bangladesh (Meezanur Rahman, pers comm. 2022).
In more recent years, Vietnam established a commercial Artemia The potential for human nutrition is excellent if the fatty acid pro-
43
production operation, mainly in salt pond systems. However, South- file of the Artemia can be manipulated after growing them intensively
east Asia's integrated Artemia pond operations are not necessarily in large amounts using high-volume wastes as a food source, and then
applicable to developed countries like Australia, where labour cost is enriching them with long-chain PUFA-rich microalgae (or other rich
high, suitable farming land is either remote or expensive and involves microbial sources) just before harvest, as recommended in a prawn
strict approvals for any venture using waste. hatchery study.15 The fatty acid composition of Artemia sp. is primar-
An example of an intensive pond production system used mainly for ily determined by the food it ingests and the nutritional quality can be
biomass production, like vinasse application in Philippines, is the commer- improved by dietary manipulation just before feeding the Artemia to
cial Artemia system in Thailand, which uses ‘ami-ami’ as feed. ‘Ami-ami’ is the consumer. The nutritional value of ongrown Artemia can be supe-
the waste obtained in the industrial production of monosodium glutamate rior compared to freshly hatched nauplii, which could be affected by
(MSG), a food flavour enhancer commonly used in Asia.44 MSG is pro- unpredictable changes to the natural environment.
duced by fermentation using a culture of bacteria with carbohydrates Because of their capacity to grow fast and frequently reproduce
sources, like tapioca and molasses. The waste ‘ami-ami’ is a dark coloured on SCP produced from agricultural waste and by-products, the poten-
viscous liquid, that is further fermented for weeks to months before being tial of Artemia as fishmeal replacement is high.
applied to ponds. Production yields in these Artemia biomass farms in Recently, research and publications on Artemia have generally
Thailand reach over 100 kg per ha per day.45 decreased.
‘Ami-ami’ is similar to an MSG by-product used in a study in the Figure 2 summarises the number of publications showing various
10,46
Philippines in the late 1980s, although in that study aerobically agricultural wastes to produce Artemia in different outdoor pond sys-
digested sugar mill vinasse and liquid manure showed significantly tems that reached commercial scale or are now ongoing. Countries
superior performance to the MSG by-product and unaerated vinesse shown are only those where the development of Artemia production
T A B L E 2 Summary of publications on use of agricultural waste for Artemia culture, with emphasis on biomass production, and evolution of culture techniques and set-up from traditional
1164
systems to high-volume waste usage of vinasse for SCP production in outdoor/pond systems.
Culture set-up/
Years Agricultural waste/by-product used Country technique Products References
Outdoor/pond culture
1960s Bird droppings (natural productivity) San Francisco, United Commercial salt pond Salt and Artemia cysts (former global cyst supplier) Authors' observation
States (1980–1984)
1979 Manure for Fertilisation Philippines Commercial salt pond Salt, Artemia (5 kg cysts/ha/month at dry season) 39
1980–1983 Chicken and cow manure as fertiliser Philippines Pilot-scale integrated Artemia, milkfish, salt 10,47,48
Artemia-salt pond Cyst = 7.45 kg/ha/month
system Biomass = 154 g/sq m in dry weight
1980–1985 Chicken manure as fertiliser weekly or Thailand Experimental, then scaled Artemia/salt/fish: ave. of 25 kg/ha/per month wet 49
as needed up to commercial in cysts in 1980, shift to biomass increased from
Artemia-salt, Artemia- 1983, with 86.4 tonnes total wet biomass in
salt-fish, or 1984
monoculture of
Artemia
1982 Chicken manure with rice hulls (sacks in Vietnam Experimental salt ponds— 6.8 kg dry wt/ha/month 50
ponds) ‘semi-intensive and Artemia cysts
static’
1984 Rich mangrove water supplemented Brazil Solar Salt Ponds/large Salt, Artemia (30,800 kg down to 1240 dry 51
weekly with chicken manure fertiliser Salinas, with few cysts/year by end of declining harvest)
experimental ponds
1984–1988 Poultry flow-through green water Philippines Commercial, 20-ha Chicken egg, salt, milkfish, shrimp, sea bass, 10,40,41,48
coming from reservoir below the integrated poultry-flow mangrove snapper and Artemia (20 kg dry cysts/
poultry which flows through through system, ha/month and daily biomass standing crop of 2–
increasingly saline ponds Artemia inoculated at 7 tonnes/ha, with 1%–5% harvested to feed
+ aerobically digested cow manure in stocking density of chicken layers and tiger prawns daily); first
seawater, for SCP production, as 50/L record of continuous culture through rainy
direct food source if microalgae-rich season using overflow pipes
water is insufficient
1986–2018 Green water from adjacent ponds; Vietnam First inoculation trial of Salt; Artemia cyst production 7 (to be updated in
chicken manure (producing Artemia in saltworks, • Intensive system: 150–250 kg WW/ha/season 2023)45
Cyanophytes); direct pond commercialised over (3–4 months/season)
supplement: rice bran, chicken the years • Extensive system: 50–70 kg WW/ha/season
manure Artemia Biomass production
2018 ami-ami (monosodium glutamate [MSG] • 2–4 tonnes WW/ha/month
derivative)
1987 Marine bird manure applied monthly as Peru Experimental evaporator Artemia cysts (wet weight basis: 1.3 kg/ha/day for 52
fertiliser pond 13 days) and biomass (wet weight 60 g/cu m for
48 days or 24 g/sq m)
OGBURN ET AL.
TABLE 2 (Continued)
Culture set-up/
Years Agricultural waste/by-product used Country technique Products References
OGBURN ET AL.
1988–1989 Aerobically digested sugar mill vinasse Philippines Commercial 60-ha Salt, milkfish and Artemia (30 kg dry cysts/ha/ 10,46
+ cow manure in seawater; MSG by- integrated intensive month and daily standing crop up of 7–10
product tested but not commercially Artemia salt pond tonnes/ha, variable harvest (for use in tiger
used as vinasse gave superior result system in a 1000-ha prawn hatchery up to 1% of biomass daily)
farm, Artemia
inoculated at stocking
density of 50/L using
1987 Philippine cysts
1988–1991 Algal-rich fishpond effluent, chicken Israel Large experimental ponds Artemia: Average 5 kg/1000 m2/day of biomass for 53
manure fertiliser and micronised soy few
protein supplement months; Over 2 kg of dry cysts/1000 sq m/month
1989–1990; 1992 Dry chicken manure Bangladesh 1000 m2 salt pond with 1639.9 g (dry wt) of cysts 54
45 m2 Artemia culture
1990–1993 Chicken manure, aerobically digested Philippines 2-ha integrated Artemia- Use of sugar-mill waste-fed Artemia to wean 10,42
sugar-mill waste (vinasse) grouper commercial grouper larvae and on grow them for weekly
fishpond system export to Hongkong or to supply local
restaurants
1991 MSG derivative, chicken manure for Thailand Seasonal solar salt farms 10–20 kg dry weight (dw) cysts and/or 100 to 55
phytoplankton bloom before stocking 375 kg wet weight (ww) biomass/ha/month
Artemia
1994 Endemic bird excrements (guano), pond Peru Commercial salt ponds Artemia biomass and enriched, frozen Artemia to 56
detritus, Ulva lactuca pruned by males feed shrimp broodstock in hatcheries.
2000–2018 Ecuador Commercial salt ponds 200–300 pounds per hectare per month
0.25-ha recirculating 4000–18,000 kg Artemia biomass per month.
ponds
2002 Chicken manure, sieved before aerobic Mexico Experimental ponds Artemia biomass 57
fermentation
2002–2003 Mixture of Torula yeasts and micronised Israel Experimental Artemia biomass, average of 40.28 ± 4.84 kg m 3 58
soy protein after initial microalgae interconnected series (wet weight) in 600 L and 31 kg m 3 in 3000-L
feed of four 600-L to tanks after 17–20 days
1000-L tank and pilot
system of three
2000-L to 5000-L
tanks
2009 Pig manure (PM), rice bran (RB), Vietnam Experimental ponds, Artemia: Average 1.8 and 2.3 tonnes wet weight 59,60
combined PM + RB, combined PM, adjacent green water ha 1 biomass
and soybean meal and green water (manure fertilised) with 1.587 kg/ha, highest biomass harvest in 3-day
(pig manure fertilised) supplemental feeding harvest intervals
directly applied or in
sacks
1165
(Continues)
1166 OGBURN ET AL.
systems was introduced in managed salt farms or specifically designed

set-up, from artisanal to intensive commercial level for local use and
import markets. Indoor systems are not included since, until now,
there are no known established commercial indoor production sys-
References
tems. One report may cover several years in a given country, indicat-
61,45
ing the scarcity of publications since the 1980s, especially those
44
59
62
focused on high-volume waste utilisation for Artemia.
It is important to note that although there may be limited publica-
Artemia biomass production: 4.5 metric tonnes/ha/

1500–3000 kg wet weight/ha/month in Thailand's
tions available according to when each country conducted trials or

research, the potential for commercially producing Artemia cysts or bio-
Artemia: 27.8–51.9 kg wet weight ha 1 cyst;
Average 2.2-ton wet weight ha 1 biomass
mass profitably is already clearly demonstrated from the reports
• 75% local use, 25% exported frozen

reviewed. Remediating agricultural waste through the production of
MSG-waste-fed developed ponds
nutrient-rich Artemia could potentially be an approach to achieving a cir-

cular economy that could also help alleviate the problem of protein short-
age. The use of Artemia as potential fishmeal replacement has been also
Artemia cyst and biomass
Artemia cyst and biomass
recommended in a study using algal fed Artemia culture in tanks (brine

shrimp bioreactors) as part of an integrated marine production system.64
Products
month
4 | DI RE C T AN D I N D I RE C T US E OF
NA
AGRICULTURAL WASTE IN ARTEMIA

PRODUCTION
direct feed supplement
Experimental ponds, with
pond cultures in China
Vietnam and Thailand

Asstd. sizes commercial
60-ha semi-intensive
Section 3 has shown different methods of using agricultural wastes in

ponds systems in
Commercial ponds
Commercial ponds
Commercial ponds
Twelve 300-sq m
Artemia production. A closer look at these systems is presented in this

Culture set-up/
section, but discussion will be limited to outdoor production because

technique
there is no documented commercial scale operation of growing Arte-

mia biomass in indoor systems yet.
4.1 | Direct addition of waste as fertiliser

Thailand case
China, Vietnam,
Bangladesh
Direct addition of agricultural waste, like solid manures, to the Artemia

studies
Thailand
Vietnam
Vietnam
Country
production area is usually done as part of the pond preparation to

increase the organic matter of the soil and then followed by inorganic
fertiliser once the water is deep to promote phytoplankton growth, as
discussed in some of the publications using manure as given in
tapioca, pig manure—carbon source in
phytoplankton, wheat flour, molasses,
in Vietnam; MSG waste up to 100 L/
Chicken Manure—mainly as fertiliser in

bran and soya pellets as supplement
manure as fertiliser: micronised rice
Table 2. However, it is difficult to maintain sufficient algal bloom to

Agricultural waste/by-product used
‘green water’ ponds for supply of

Pig manure (PM) and rice bran (RB–
Assorted waste, including chicken
provide natural food for Artemia in the widespread traditional use of

fermented in alcohol yeast) as
supplement to green water
chicken manure in Artemia ponds as direct food or fertilisation ponds

to stimulate algal growth, followed by pumping ‘enriched water/green
biofloc development
water’ to the culture ponds.60 Hence, inert diets, like rice bran, have
day/ha in Thailand
been applied in the culture pond as a food supplement.

MSG derivative
The problem with relying on the natural productivity of the cul-

ture area is that Artemia can easily consume natural food and a contin-
uous supply must be provided. In a review on feeding as one of the
NA
(Continued)
most important factors affecting Artemia production (see Table 2), the
inadequacy of traditional methods used in ponds to promote phyto-
plankton bloom using fertilisers supplementation with cheap agricul-
2012–2013
tural waste products and chicken manure directly applied in the pond
TABLE 2
was discussed.62 These methods often result in suboptimal feeding

Years
2015
2018
2018
levels and high nutrient pond effluent discharges. Hence, the authors
recommend using biofloc technology for Artemia production.
OGBURN ET AL. 1167
FIGURE 1 Overview of the use of agricultural waste and by-products to produce Artemia in indoor and outdoor systems.
4.2 | Biofloc technology pathogens, introduction and improving the farm biosecurity, enabling
aquaculture to further develop an environmentally friendly
Biofloc technology is based on the principle of waste nutrients recy- approach.67
cling, particularly nitrogen, into microbial biomass that can be used in The increasingly popular approach to managing ponds using bio-
situ by cultured animals or be harvested and processed into feed floc systems in aquaculture is widely discussed.37,68,69 This involves
65
ingredients. Heterotrophic microbiota is stimulated to grow by providing a nutritious food source that promotes higher productivity
steering the C/N ratio in the water through the modification of the or higher nutrient in an integrated aquaculture system. These studies
carbohydrate content in the feed or by the addition of an external car- followed after it was reported that bacteria could be used as a nutri-
bon source in the water, so that the bacteria can assimilate the waste ent source for Artemia to compensate for suboptimal algae supply
ammonium for new biomass production, eliminating the need for when molasses supplementation resulted in much lower total Artemia
water exchange. biomass compared to significant improvement when beneficial bacte-
In the review recommending the use of biofloc technology,62 the ria were combined with molasses.70,71
formulated feed developed specifically for Artemia pond production Although biofloc development to increase Artemia production
involved adding tapioca flour or molasses as the carbon source to and improve pond water quality has been well reported, the applica-
obtain the ratio C/N ≥10 to stimulate bio-floc development as feed tion may only be suitable for the addition of limited volumes of
for Artemia. Biofloc application is related to using SCP in aquaculture waste/by-products as carbon source (e.g., molasses), or the use of a
to reduce feed costs by minimising the need for expensive protein more refined source of cellulose, but not for direct addition of high
components through microbial protein synthesis.66 To remove the COD-waste, like sugar-mill and distillery vinasse, with at least
problem of harvesting and processing microbial cells, they tested 30,000–40,000 mg/L COD46,72 as abundantly found in some coun-
directly in situ production of SCP in continually mixed and aerated cir- tries like Australia.
culated fish ponds, with daily addition of cellulose or cereal meal, like The lower Artemia biomass obtained using molasses supplemen-
sorghum. The carbon source provided the substrate for SCP, with tation in a biofloc system may be caused by its direct application to
nitrogen coming from the pellets or ammonium sulphate supplements. the Artemia culture without aerobic digestion first to promote SCP
A comprehensive review of Biofloc use for aquaculture applica- growth.70,71 Direct addition of the cellulose or carbon source to a cul-
tions and the animal food industry summarises the advantage of the ture, even in combination with beneficial bacteria, has to be well regu-
technology in minimising consumption and release of water, recycling lated and best applied to lower COD sources, such as the use of
in situ nutrients and organic matter, reduction in introduced cellulose or cereal meal (e.g., sorghum).65 However, said materials
1168 OGBURN ET AL.
F I G U R E 2 Artemia production reports in outdoor pond systems using various agricultural wastes in countries where commercial trials or
business has been established.
could be more costly as they have other uses in the livestock, or other through a simple pipe overflow system design that enables mainte-
developed industries, unlike high-volume waste that are still primarily nance of higher salinities at 60–80 g/L to exclude predators and com-
disposed of or stored long to get remediated and pose an environ- petitors that generally start to inhabit the culture ponds in the wet
mental risk if leached. season, as summarised in Table 2.These high biomass production sys-
The disadvantages of the Biofloc system have been summarised tems result in a multiplier effect on profits.10,40,48
73
in a review, suggesting that producers better adopt a closed man-
agement system for biofloc ponds and have a compartmental design—
where fish production and microbial proliferation occur in separate 4.4 | Aerobic digester system for SCP production
spaces—to make management easier. This separate waste processing
compartment has already been proven very effective in the saline The use of a separate aerobic digester to produce SCP adjacent to the
waste processing pond or aerobic digester designed for intensive Arte- Artemia culture, prior to the addition of liquid feed to the Artemia pond,10
10,41
mia production in the Philippines, as discussed further in this makes addition of beneficial bacteria inoculum unnecessary. A readily
section. available SCP sustains continuous high Artemia biomass production. Bio-
remediation of the waste to manageable nutrient levels improved the
physico-chemical and biological parameters before adding SCP daily to
4.3 | Integrated poultry/livestock Artemia systems the Artemia culture at regular hourly intervals through regulated faucets
and piping. This is shown during preliminary trials in Australia using dun-
Integrating poultry or livestock into an Artemia salt pond sys- der wastes from bioethanol and rum production when aeration for 3–
tem10,40,41 in flow-through system enabled continuous supply of phy- 15 days continued to lower the BOD while increasing SCP in the digested
toplankton and other SCPs to feed Artemia as well as utilisation of waste used to feed Artemia.74 The production of SCP that can be directly
several crop by-products and other waste in feed manufacture for the utilised by Artemia is a more sustainable way of utilising waste.10,41
poultry or livestock. The SCP in this system is produced separately The use of SCP as a potential solution to the increasing food pro-
from the Artemia pond because the waste goes to a reservoir below tein demand in the World has long been recognised, studied, docu-
the poultry or in the waste sump adjacent to the livestock and flows mented or reviewed.75–80 Authors roughly define SCP as the dried
or is hosed to the Artemia pond already aerobically converted to SCP, cells of bacteria, algae, yeast and fungi, rich in proteins and could be
similar to the digester discussed in the next section. A standing crop used as a dietary supplement after growing using various substrates,
of 7 tonnes/ha can be maintained daily in a poultry flow-through/ mainly agricultural wastes. They are mostly dried because harvesting
livestock system, although optimum daily harvest was not determined the tiny cells of 10-micron or below in enormous tonnage is still an
since harvest was on as needed basis for prawn or poultry supple- expensive process, if not a logistic impossibility, to be used fresh as
ment. Artemia production could even be extended to the wet season the protein source.
OGBURN ET AL. 1169
Among the advantages of growing SCP is as a nutrient supple- associated with low pH and high COD. Hence, they must be disposed
ment for humans because it contains not only protein but carbohy- of properly. The existing process is either to bury the waste in unpro-
drates, fats, water and other elements, and its requirement for growth ductive private lands or to apply a more costly, complex process
is not as limiting as those for animals and plants because it is neither involving anaerobic and aerobic treatments, requiring additional infra-
seasonal nor climate dependent. However, SCP production is still min- structure for existing operations. In Southeast Asia, river or coastal
imal and has not risen in proportion to rising protein food demand. waters sometimes become the disposal site of significant amounts of
Moreover, its production, which usually involves anaerobic fermenta- waste, for example, sugar mill washings, with deleterious effects on
tion, is relatively costly and capital intensive, harvest is not easy, the environment, including fish kills that can deprive marginal commu-
improvements in quality is required to remove potential toxicants or nities of a food source.82
health hazards for human, its acceptability needs to be increased, and Poultry and livestock (feedlot and dairy) also produce high volume
palatability may need to be enhanced. There are suggestions of the wastes that are proven effective in Artemia biomass production, as
need to make genetic improvements in producer organisms. shown in Tables 1 and 2, however, the wastes have other significant
Production of Artemia using SCP grown in a simpler and cheaper use as fertiliser, especially for the horticulture industry in Australia.
aerobic digestion setup is an attractive alternative to producing SCP Manure supply from the biggest poultry producers in Australia is
directly for human consumption, unless it involves high-value prod- already contracted in bulk for horticulture use (Baiada and Inghams
ucts, as currently used in nutraceutical industries, like the production Enterprises, pers. comm., 2018). Livestock manure is often reused to
of nutritious microalgae that makes capital and operational cost sus- fertilise paddocks or horticulture. These wastes can also be easily
tainable. Biofloc technology for Artemia also uses SCP to create a dried, packed, stored or transported.
healthy nutrient balance in ponds; the difference is that the reaction Because the use of high-volume sugar-based vinasse waste for
is done directly in the ponds by adding cellulose and bacteria, which is intensive Artemia production has only been reported in one commer-
more difficult to control compared to a separate SCP producing aero- cial salt farm in the Philippines,10 there are few examples of how sugar
bic digester. The digester removes the need to closely manage the and alcohol production-based wastes are currently treated. Figure 3
Artemia culture pond, or add bacteria as required in the biofloc tech- shows a simplified diagram of where waste can be sourced in
nology. SCP that is pumped daily from the aerobic digester is con- Australia's alcohol and sugarcane-based industries, with potential as
verted to biomass immediately by Artemia. SCP food source for Artemia. Only wastes that pose a challenge for
Because Artemia is a shrimp and tastes like any prawn or shrimp disposal and used as fertiliser or as a livestock food supplement, are
when cooked, its acceptability may be easier to address, especially in included here, such as dunder and vinasse.
developing countries, like Bangladesh and Vietnam,63 which now uses For the wine industries, the waste is mainly a collection of wash-
Artemia biomass as a replacement for other crustaceans in making ome- ings from various processing activities often directed to a holding/
lettes than using SCP as direct human protein source. Analyses of waste storage area and allowed to aerobically decompose before use as pad-
can address any concern on safety and the quality of Artemia produced, dock fertiliser or disposed of on land. This effluent could vary highly
for example, through metabolomic, nutrient and heavy metal analyses. from farm to farm. Bulk waste from a crushed grape, known as marc,
A higher standing crop of 10 tonnes/ha was obtained in the inten- is not included in this review, rather the focus is on liquid wastes that
sive system explicitly designed to use high-volume vinasse or washings are harder to store, pack or transport in significant volumes.
from a sugar mill in the Philippines. Because Artemia harvest to provide In breweries, relatively high protein mash collected after separa-
live food to a prawn hatchery was on as need basis, optimum daily har- tion from wort brew, and the spent yeast resulting from fermentation,
vest could not be assessed. Whether the maximum Artemia daily stand- are a potential medium for growing microalgae or as SCP food source
ing crop can go higher than 10 tonnes/ha in such a system could not be for Artemia.
determined either because vinasse was provided from another island. In sugar cane-milling, a direct sugar-base that could be used as an
Feeding was limited by how much waste could be transported. SCP medium for Artemia is low-grade molasses. However, farmers
already buy it to re-fertilise sugar cane or other crop farms or use it in
livestock feed preparation.83 Hence, remediation is not as pressing an
5 | AUSTRALIAN CASE STUDY: issue as other high-volume wastes like vinasse.
P O T E N T I A L OF U S I N G S U G A R - B A S E D In Australia, farms generally refer to the concentrated waste from
WAST E FO R A R T E M I A P R O D U C T I O N T O molasses-based alcohol production as dunder, also known globally as
H E LP R E M E D I A T E P O LL U T A N T S stillage or vinasse. Wilmar Bioethanol, the only Australian company to
operate the Biostil process, produces a more concentrated dunder
Sugar-milling, bioethanol and rum production from sugar or molasses, stream, referred to as BioDunder, than molasses-based rum distiller-
and wine and beer production are significant agricultural industries ies.84 This liquid by-product of ethanol contains approximately
around the World. An estimated 191.2 million L of pure alcohol are 30%–40% solids, comprising vegetable matter (yeast biomass) with
available for consumption from alcoholic beverages in Australia, with potassium, sodium, nitrogen, calcium, magnesium, phosphorous and sul-
39% contributed by beer, 38.6% by wine and 19.9% by spirits/ phur. It is also useful as liquid fertiliser, although significant volumes are
RTDs.81 These industries produce a significant volume of waste, often left unused and stored in ponds, awaiting technology for further use.
1170 OGBURN ET AL.
F I G U R E 3 Simplified diagram of waste sources in the alcohol and sugarcane-based industries (Based on information taken during visits to
Australian sugar mills, rum/bioethanol distilleries and beer and wine production facilities).
Distilleries that produce alcohol using fresh sugarcane juice processes or multi-stage treatments for both anaerobic and aerobic
(e.g., Agricole rum) or from heated sugar syrup, raw or dextrose sugar, phases, including a decolouration step, for the effluent to be reused
produce waste vinasse. or safely disposed of.
In a review of approaches to distillery wastewater, effluent from Treatments involving anaerobic and aerobic processes may be
distilleries or spent wash is considered an extensive soil and water more beneficial for companies that invest in infrastructure to treat
pollutant.85 Spent wash is described as highly acidic (pH 4.0–4.3) with waste for fuel production (e.g., methane from the anaerobic phase),
high rates of biochemical and chemical oxygen demand (BOD: 52–58, but not all distilleries are equipped for complex treatment processes
COD: 92–100 kg/m3) and suspended solids (2.0–2.5 kg/m3).86 In that would add to the cost of the operation. Thailand uses the anaero-
Brazil, vinasse is often used in fertilisation and irrigation practices, bic treatment of MSG successfully for commercial Artemia production.
72
referred to as fertirrigation, which may be linked to adverse environ- A more straightforward approach, like direct aerobic digestion of
mental outcomes if an excess is applied.87 spent wash/vinasse/stillage to produce SCP as food to grow the
Anaerobic digestion is widely accepted as the first step in treating highly fecund brine shrimp, can be an alternative with economic bene-
distilleries spent wash or sillage followed by aerobic processing, aimed fits. Even if bacterial, fungal and phytoremediation treatments are
88
at getting biogas and reducing the polluting effect. However, in the used to produce species with high values, as shown in Table 3, the
absence of such complex treatment set-ups in many distilleries, a problem of mass harvesting relatively minute organisms in larger vol-
promising alternative is to use a simple, aerobic-digester to grow SCP umes could still pose problems. The microscopic SCP resulting from
that can be used as food to produce intensive Artemia biomass and direct aerobic digestion of relatively concentrated distillery wastes
10,46,74
remediate a potential pollutant at a faster rate, as discussed in can be easily consumed by Artemia to produce a high quantity of bio-
the previous section. mass that is easier to harvest, process and transport.
Table 3 summarises examples of studies on the treatment of An important consideration in using high-volume sugar-based
high-volume wastes from the sugar and alcohol industries, focusing alcohol waste to produce Artemia in Australia is that 5.7 million hect-
on spent wash or vinasse. The table shows that various methods have ares of land in the country have become unproductive for conven-
been used to treat winery, brewery and distillery wastes. However, tional agriculture due to increasing salinity levels, arising from
the problems in treating large volumes of distillery effluent containing traditional farming methods introduced by man. This caused a marked
recalcitrant compounds, including the difficulty of removing the dark deterioration in the quality of surface waters, which led to the estab-
83
colour with anaerobic treatment, are well documented. Therefore, lishment of large-scale evaporation basins as an engineering
conventional wastewater treatment methods may not be sufficient response.31,89 Although several research and commercial
for distillery effluent and the suggested treatment is a combination of ventures have been conducted using inland saline aquaculture in
OGBURN ET AL. 1171
TABLE 3 Some examples of bioremediation studies done on high-volume agricultural wastes, with emphasis on sugar and alcohol-based
industries.
Agricultural waste/ Waste production processes/treatment/

Years by-products Country Industry studies References
2002 Molasses distillery India Cane molasses-based Biogas recovery by bio-methanation, followed 85
wastewater/spent wash distillery by multiple effect evaporators and bio-
composting
2005 18 assorted winery effluent Spain Winery and distillery Waste characterisation to determine feasibility 92
and 13 distillery vinasse for agriculture use
2007 Distillery wastewater, with India Distilleries Toxicity profile, colourants, and treatment of 84
focus on coloured spent spent wash by anaerobic or aerobic methods
wash (bacterial, fungal, mixed consortia and
phytoremediation)
2007 Distillery wastewater/spent India Distilleries Ozone pre- and post-aerobic treatment versus 93,94
wash conventional aerobic Digestion only;
thermal/anaerobic pre-treatment, advanced
oxidation techniques, ultrasound, ozone to
enhance aerobic oxidation
2008 Wine-related wastewaters South Africa Winery Fungal and enzymatic remediation 95
2008 Spent brewer's yeast Turkey Brewery Induced autolysis at elevated temperature to 96
produce yeast extract
2011 Bagasse/grape marc, lees Spain Winery Trim wastes, grape marc, and wine lees for 97
production of lactic acid and bio-surfactants
2011 Assorted wastes, with focus Australia Winery Primary/Secondary/Tertiary Treatment 98
on winery wastewater Technologies, including Aerobic and
Anaerobic Treatment, use of evaporation
ponds and wastewater bioremediation cell
(WBC) being trialled for smaller wineries
2011 Molasses-based raw India Molasses-based industry 99
industrial effluents
2012 Distillery wastewater India Alcohol distilleries Need of cost-effective treatment scheme, using 100
bio-methanation as primary step, followed by
physicochemical treatment and ending with
aerobic treatment. Also need further research
on emerging method like enzymatic
treatment.
2012 Distillery effluent India Alcohol distilleries Phycoremediation using the green microalga 101
Scenedesmus sp
2013 Distillery vinasse Brazil Sugar-ethanol industries Fertirrigation, concentration by evaporation, 86
energy production; the effects on soil
physical, chemical and biological properties;
its influence on seed germination, its use as
bio-stimulant and environmental
contaminant. Green methods need to be
developed
2014 Vinasse Brazil Sugarcane bio-refineries Anaerobic digestion of vinasse to produce 102
biogas for electricity or vehicular fuel
replacement or alternative to diesel; Biogas
in cogeneration to release bagasse for
second- generation ethanol production
2014 Spent wash India Cellulose-based ethanol Anaerobic methane production; reverse 103
industry osmosis; melanoidin degradation by
phycoremediation
2014 Vinasse Brazil Sugarcane alcohol Various fungi (Pleurotus) cultured in vinasse as 104
supplement feed for Danio rerio fish; non-
toxic
2015 Vinasse Brazil Ethanol distillery Biodegradation of sugarcane juice vinasse in 105
aerobic and anaerobic conditions
(Continues)
1172 OGBURN ET AL.
TABLE 3 (Continued)
Agricultural waste/ Waste production processes/treatment/

Years by-products Country Industry studies References
2016 Vinasse from Sepahan Bio- Iran/Sweden Molasses to Ethanol Edible fungi Neurospora intermedia and 106
product Company Isfahan, Company Aspergillus oryzae has grown in diluted
Iran vinasse, to produce 223 g of fungi per litre of
vinasse
2017 Brewery wastewater United States Brewery COD treatment by continuous flow microbial 107
fuel cell (MFC) treatment system, with no
catalyst
2019 Vinasse Brazil Ethanol from sugarcane Ozone treatment + anaerobic digestion 72
or molasses (biogas), + aerobic growth of fungi reduces
COD by 95%, total removal of phenols and
>80% of total N
Australia,31,35,89–91 it has remained mainly on a practical level or an 6 | A P P L I C A B I L I T Y OF V A R I O U S S YS TE M S

on-and-off commercial venture. T O U T I L I S E WA S T E F O R A R T E M I A
Little has been done to commercialise live food more suited to PRODUCTION
inland saline areas, except for Dunaliella and Artemia in Western
Australia,35 a commercial operation in South Australia and a pilot Systems to produce Artemia using agricultural waste vary according to
operation in Northern Victoria that showed potential for Artemia pro- country and what resources are available.
duction and marketing,31 none of which have resulted in a sustained Table 4 evaluates the different systems of using agricultural
continuous commercial venture. From the literature, it is apparent that waste for Artemia production based on different factors relevant to a
either the species trialled in inland saline areas are unsuitable to the sustainable industry. A simplified version of significant factors, pat-
extreme conditions, the set-up or operation is not designed to operate terned after the One-Health Lens approach,108 is illustrated in
as a highly profitable integrated venture or intensively with optimum Figure 4 to help those needing to decide which system is best suited
feed input- harvest output as has been established in Asia, where dis- for their purpose and area of Artemia production. The factors are
tinct wet and dry season affects Artemia production. rated from 0 to 5 based on Table 4.
Feed studies using waste or microalgae to grow Artemia have If the quality of Artemia is enhanced before harvest and toxicants
shown that failure to sustain continuous production, in conditions are not shown in the product, there is potential for the use of Artemia
where predation is not much of a threat, is often associated with in human nutrition, aside from being a candidate to replace fishmeal
decreasing food availability, as is the case in salinas,51 and some salt to address the increased demand for protein sources in the fast-
ponds relying on natural productivity, where Artemia production has growing aquaculture industry. A high-volume waste, like rum dunder,
reduced over the years as nutrients eventually deplete. is relatively sterile when leaving the distillers, and microbial compo-
With high-volume waste, like vinasse, remaining a pollution chal- nents that grow in the holding tanks are generally Lactobacilli, which
lenge to many countries, if not properly treated, the merger of two are relatively safe. Some dunder is even reused in the rum operation
industries, aquaculture with its highly nutritious all meat brine shrimp to minimise water usage, as shown in the microbial ecology of the
Artemia, and agriculture where remediation of high-volume of waste Bundaberg rum production process.109
is still an environmental challenge, may prove to be a great opportu- Figure 5 shows the various culture systems using waste to pro-
nity for food production. Liquid waste can provide the much needed duce Artemia, illustrating a simplified input–output flow as a further
SCP and Artemia, the natural harvester that solves the decades-old guide to deciding on a design to suit different areas and product
problem of processing minute protein cells for sustainable continuous requirements.
protein production. Managed production of Artemia using waste also
eases the reliance on approximately 90% of Artemia harvest from
inland salt lakes that are under constant threat of drying up due to cli- 7 | SUMMARY AND CONCLUSIONS
mate change, as observed in many lakes over past decades.9
Considering that inland saline areas in Australia are spread across Many agricultural industries produce significant volumes of wastes
a large area in many states where there is likely to be a distillery, win- that are underutilised, disposed of, or put on land as fertiliser that may
ery or brewery with high volumes of waste needing remediation, it cause pollution due to their high nutrients, especially if accumulated
would be a worthwhile venture to see how far the production can be over time beyond any possible initial fertilisation benefits. Treating
optimised if there is a continuous supply of waste available for aerobic these high-volume wastes with conventional methods for industrial
digestion to supply food to Artemia in areas where very few other wastewater, involving multiple steps of anaerobic and aerobic treat-
aquaculture species can survive. ment processes, would be uneconomical for those traditionally storing
TABLE 4 Comparison of various waste remediation techniques using Artemia or involving high-volume wastes: applicability, constraints and potential
Waste as direct Waste as nutrient source in SCP production from aerobic Anaerobic or combined anaerobic
Technology criteria fertiliser integrated farming system Biofloc system digestion of agricultural waste and aerobic treatment of waste
OGBURN ET AL.
Waste used Poultry and livestock Poultry and livestock (flow- Molasses, tapioca flour, with Poultry, livestock, sugar and MSG derivative (as used in
through for enrichment; nitrogen coming from alcohol production waste— Thailand); anaerobic-aerobic
not using separate pellet waste or other vinasse, dunder and bio- treatment used traditionally to
digester) nitrogen source in the dunder treat vinasse
culture
Intensity of operation Extensive aquaculture Extensive to intensive Extensive to semi-intensive Semi-intensive to intensive Intensive
systems
Cost Low Low to medium (acc. to Low to medium (bacteria Low to medium (high-volume High (involves various equipment
poultry/livestock intensity) + cellulose to balance N) waste sourcing if not and materials in different
produced nearby) stages)
Labour Low High Low to medium Low Medium to high
Optimised water Low High High (if C/N/microbial High (SCP converted to Artemia Low to medium
usage/quality balance maintained) biomass quickly)
Use of chemicals/ None Low to medium (poultry Low to medium None High
supplement only)
Management/ Low Low to medium (mainly Low to medium (balancing Low (automated, SCP pre- High
operation complexity poultry management) chem ratio for SCP in situ produced)
production)
Income generation Low High Medium to high High High (if fuel and valuable microbes
produced)
Low as treatment only
Sustainability/ Low High Medium to high High Medium
optimised farm
system
Reducing carbon Low High High High Medium (if fuel produced but
footprint complex processes may result
to increased footprint)
Potential to remediate Low Medium to High (indirect Low (C/N/microbe balance is High (aerobic digestion outside High if complex operation is offset
high volume of remediation through use hard to maintain, esp. with the ponds lowers polluting by fuel and special microbe
waste of waste for poultry/cattle high nutrient waste) nutrient and mainly SCP goes production
feed) to pond)
Abbreviations: MSG, monosodium glutamate; SCP, single cell protein.

1173
1174 OGBURN ET AL.
FIGURE 4 Comparative analysis of different waste processing systems for Artemia production using a modified One-Health lens approach.108
FIGURE 5 Simplified diagram of different outdoor production systems of Artemia and their input–output flow for waste processing.
or holding excess waste in private lands other than what they use for dependence on Artemia importation or cut costs in the aquaculture
fertilisation. Better ways are needed to remediate waste beyond the and aquarium industries. Furthermore, the more straightforward pro-
nutrient capacity of their crop production areas. cess of SCP production by aerobic digestion instead of a more costly
Using sugar and alcohol-based wastes in the intensive production and complex method of using multi-stage anaerobic/aerobic pro-
of the brine shrimp, Artemia, in indoor or pond production systems is cesses will boost sustainability in distilleries that are not equipped
potentially a solution to two major global problems: bioremediation of with specialised waste treatment facilities, and promote a circular
high-volume agricultural wastes and production of nutritious feed/ economy where waste becomes a resource. Because of the simpler
food to address the global protein shortage. This can minimise set-up, the system applies to any country.
OGBURN ET AL. 1175
For less developed countries, where marginal coastal communities Newcastle, as part of the Wiley - The University of Newcastle agree-
rely on harvesting the diminishing resources of the sea for subsistence, ment via the Council of Australian University Librarians. [Correction
an integrated poultry/livestock-Artemia-fish/crustacean flow-through added on 3 February 2023, after first online publication: CAUL fund-
system may be an excellent alternative to address socio-economic con- ing statement has been added.]
cerns since the system can provide a multiplier effect on profits and a
much-reduced carbon footprint. CONFLIC T OF INT ER E ST
The use of multi-stage or complex processes to remediate The authors declare no conflicts of interest.
high-volume waste is best limited to bioremediation aimed at pro-
ducing high-value products, for example, microalgae with highly DATA AVAILABILITY STAT EMEN T
specialised use, like the production of biofuels and nutritional sup- New data were not created nor analysed in this review, so data shar-
plements where the end product can pay for the cost of treatment. ing is not applicable.
Although there are no publications describing details of the
process used in feeding the waste product of MSG production, OR CID
‘ami-ami’ to Artemia, Thailand has successfully produced Artemia Nepheronia Jumalon Ogburn https://orcid.org/0000-0002-0060-
biomass commercially for many years, with daily production of 2808
10–50 kg/ha, equivalent to 340 tonnes/year,110 which is currently
updated in a forthcoming publication to 100 kg (average) per ha of RE FE RE NCE S
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Various systems of growing Artemia in inoculated managed ponds intensity of an illustrative subset of current and future protein
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7. Lavens P, Sorgeloos P, eds. Manual on the production and use of live
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AUTHOR CONTRIBUTIONS 10. Ogburn DM, Ogburn NJ. Experiences on integrating the use of
Nepheronia Jumalon Ogburn: Conceptualization; investigation; meth- organic wastes with saline aquaculture systems in the Philippines. In:
Kumar MS, ed. National Workshop on Wastewater Treatment and
odology; visualization; writing – original draft. Luchun Duan: Resources;
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Subashchandrabose: Supervision; writing – review and editing. Patrick 11. Hargreaves JA. The circular economy concept and Aquaculture.
Sorgeloos: Resources; writing – review and editing. Wayne O'Connor: December 14, 2020. The World Aquaculture Society 2022.
Accessed 15 May 2022; https://www.was.org/articles/Editors-
Supervision; writing – review and editing. Megharaj Mallavarapu:
Note-The-Circular-Economy-Concept-and-Aquaculture.aspx#.
Supervision; writing – review and editing. Ravi Naidu: Funding acquisi- Ynxp8uhBzIU.
tion; project administration; resources; writing – review and editing. 12. Abatzopoulos TJ, Beardmore JA, Clegg JS, Sorgeloos P. Artemia:
Basic and Applied Biology. Kluwer Academic Publishers;
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13. Dhont J, van Stappen G. Chapter 3. Biology, tank production and
We acknowledge the University of Newcastle for the HDR scholar-
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ship and other support provided to the first author (Nepheronia Juma- Feeds in Marine Aquaculture. Blackwell Science Ltd; 2003:65-121.
lon Ogburn). Open access publishing facilitated by The University of 10.1002/9780470995143.ch3
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Received: 15 June 2022 Revised: 22 December 2022 Accepted: 27 December 2022

Agricultural wastes for brine shrimp Artemia production: A

Nepheronia Jumalon Ogburn 1 | Luchun Duan 1,2 |

In recent decades, aquaculture has become the fastest growing major

Rev Aquac. 2023;15:1159–1178. wileyonlinelibrary.com/journal/raq 1159

Years Agricultural waste/by-product used Country Culture set-up/technique Products References

Years Agricultural waste/by-product used Country Culture set-up/technique Products References

Abbreviations: PUFA, polyunsaturated fatty acid; SCP, single cell protein.

systems was introduced in managed salt farms or specifically designed

Artemia biomass production: 4.5 metric tonnes/ha/

tions available according to when each country conducted trials or

mass profitably is already clearly demonstrated from the reports

• 75% local use, 25% exported frozen

nutrient-rich Artemia could potentially be an approach to achieving a cir-

Artemia cyst and biomass

recommended in a study using algal fed Artemia culture in tanks (brine

AGRICULTURAL WASTE IN ARTEMIA

Vietnam and Thailand

Section 3 has shown different methods of using agricultural wastes in

Artemia production. A closer look at these systems is presented in this

section, but discussion will be limited to outdoor production because

there is no documented commercial scale operation of growing Arte-

4.1 | Direct addition of waste as fertiliser

Direct addition of agricultural waste, like solid manures, to the Artemia

production area is usually done as part of the pond preparation to

Chicken Manure—mainly as fertiliser in

Table 2. However, it is difficult to maintain sufficient algal bloom to

‘green water’ ponds for supply of

provide natural food for Artemia in the widespread traditional use of

chicken manure in Artemia ponds as direct food or fertilisation ponds

been applied in the culture pond as a food supplement.

The problem with relying on the natural productivity of the cul-

was discussed.62 These methods often result in suboptimal feeding

Agricultural waste/ Waste production processes/treatment/

Agricultural waste/ Waste production processes/treatment/

Australia,31,35,89–91 it has remained mainly on a practical level or an 6 | A P P L I C A B I L I T Y OF V A R I O U S S YS TE M S

Abbreviations: MSG, monosodium glutamate; SCP, single cell protein.

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