Aquaculture 255 (2006) 488 – 494

www.elsevier.com/locate/aqua-online

Intensive mass production of Artemia in a recirculated system

Odi Zmora ⁎, Muki Shpigel
National Center for Mariculture (NCM), Israel Oceanographic and Limnological Research Ltd., P.O. Box 1212, Eilat 88112, Israel
Received 20 July 2005; received in revised form 1 January 2006; accepted 6 January 2006

Abstract

An outdoor closed system for intensive Artemia biomass production was evaluated. The system integrates the use of
inexpensive agro-techno products and photosynthesis to create an improved diet for culturing adult Artemia. The diet in the initial
days of culture consists of microalgae, followed by a mixture of torula yeast and soy protein. No water or solids are discharged
from the system during the entire production cycle. Waste products are recycled by bacteria, microalgae and protozoa, which
themselves are subsequently ingested by the Artemia in a continuous cycle. The final yield of adult Artemia after 17 to 20 days
averaged 40.28 ± 4.84 kg m− 3 (wet weight) in 600 l and 31 kg m− 3 in 3000-l tanks. Maximal yield was up to 47.5 kg m− 3. Food
conversion rate (FCR) ranged between 0.17 and 0.25. Survival rates from inoculation date averaged 23.3 ± 9.24%. Systems of this
type can productively supply hatcheries of finfish, shrimp and crabs with large quantities of live Artemia.
© 2006 Elsevier B.V. All rights reserved.

Keywords: Artemia; Intensive culture; Mass production; Recirculation

1. Introduction protein or whey (Lavens et al., 1980; Dobbelier et al.,

1980). Both extensive and intensive culture systems
The brine shrimp Artemia is an important component have used various culture regimes, from batch culture to
of the diet of a wide range of cultured marine species. continuous flow-through systems (Brisset et al., 1982).
Since the late 1970s numerous techniques for its mass- Some researchers have tried adopting unique systems
culturing have been tried, covering a large range of that are site-specific, with a relative advantage due to
culture sizes, degrees of intensification, water regimes location, availability of ingredients such as rice bran
and feeding sources (Tobias et al., 1980; Dhont and Van extract used in large ponds in the Philippines (Brisset et
Stappen, 2003). al., 1982), soy protein in Israel (Zmora et al., 2002), or
Large-pond extensive cultures are typically based on resources such as the algae-rich effluent water from
available natural microalgae as a food source (Zmora et shrimp ponds which was recirculated through a super-
al., 2002), while small-scale intensive cultures utilize intensive Artemia tank.
mostly by-products from the agriculture and food- These culture methods were aimed at producing all
processing industries such as rice bran, corn bran, soy stages of Artemia as live food for numerous species of
organisms in aquaculture. It has long been recognised that
⁎ Corresponding author. Tel.: +1 410 234 8890; fax: +1 410 234 advanced Artemia stages have many advantages over fresh
8896. or enriched nauplii as feed for finfish and shellfish, e.g. bio-
E-mail address: [email protected] (O. Zmora). encapsulation efficiency and nutritional value, earlier
0044-8486/$ - see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaculture.2006.01.018
 O. Zmora, M. Shpigel / Aquaculture 255 (2006) 488–494 489

satiation, energy gain, reduction of aggression and covered with a mesh filter. The mesh of the filters
cannibalism and cost effectiveness (Leger et al., 1986; was changed (150, 250, 350, 420, 500, 600 or 710
Dhert et al., 1992; Zmora et al., 2005). The aim of this work μm) as the Artemia grew (Lavens et al., 1980). The
was to test an innovative approach to mass-producing third tank was identical to the second one in size and
Artemia in a zero exchange water system. shape but no filter protected its outlet, and it was
used as a sedimentation tank. The fourth tank was a
2. Materials and methods 2.8 m2, 1000-l D-shape raceway (100 × 300 cm) with
a 200 cm long central partition. This tank, provided
The production trials were carried out at the National with intermittent aeration, was used for sedimentation
Center for Mariculture (NCM), Eilat, Israel (29°30′ N, and propagation of algae.
35° E). Four identical experimental production units and Tanks were filled with freshly pumped sea water (40 ppt,
one pilot unit were operated simultaneously. Gulf of Eilat, Red Sea) and enriched with nutrients NH4+
(0.5 mM l−1), PO4−3 (0.14 mM l−1), Fe+3 (24 mM l−1) and
2.1. Experimental unit design Si O− (0.56 mM l−1). The tanks were inoculated with 10
2 3
l of dense laboratory cultures (∼ 400–600 mg DW l−1)
Each experimental unit consisted of four tanks of each of the following algal species: Chaetoceros
with total volume of 2800 l, arranged in a row. The gracilis, Tetraselmis tetrathele and Navicula cf lenzi.
tanks were positioned as a cascade system in which In a preliminary study, these species were found to
water flowed by gravitation from one to the next support a fast growth of Artemia under the conditions of
(Fig. 1). The effluent of the fourth tank was returned the experimental field work we conducted. At the onset,
to the first tank via a 50 mm Ø polyethylene pipe aeration and airlift caused the water to circulate through all
using an air–water lift, with no water discharged tanks at a rate of 600 l h−1. After 3 days, the density of the
from the system. The first tank was a 600-l cylinder- algae was about 20 cm Secchi disk, and a film of N. cf lenzi
conical tank; its overflow outlet was covered with a covered the walls and bottoms of the tanks. At this point,
150 μm mesh filter of 8000 cm2 surface area; strong aeration in tanks III and IV was turned off, nauplii were
aeration from the bottom of the tank agitated the stocked into tank II, and water flow was reduced to 300
water. Two kilograms (0.4 kg dry weight) of fresh l h−1.
shredded macroalgae Ulva lactuca were introduced A 120-l cylinder-conical tank was used as a feeding
into this tank on the first day of each culture cycle. reservoir. In it a special dry diet developed at NCM from
The second tank was a square 600-l (100 × 100 × 60 inexpensive ingredients (micronized soy protein and torula
cm) flat bottomed tank which was stocked with 10 yeast) was suspended in tap water. Every morning, after
nauplii ml− 1 of Artemia franciscana (Great Salt Lake sampling and estimating the Artemia biomass in the culture
tank, a diet ration was prepared constituting 10% (DW) of
type). The tank was provided with vigorous aeration
the estimated Artemia
via diffusers from its bottom, and its outlet was

Artemia mass production system

I
II 600 L
III 600 L shredded
Artemia Ulva tank
IV 600 L
Sedimentation culture tank
1000 L Suspended
tank
Microalgae dry diet tank
tank Pump

Aeration Aeration

Air-water
lift
50 mm recycling pipe

Fig. 1. Schematic plan of Artemia mass production system.

490 O. Zmora, M. Shpigel / Aquaculture 255 (2006) 488–494

biomass (WW). As the Artemia grew, the ration of dry trough. The rationale for using only three tanks, instead
diet was increased proportionately and never exceeded of four as in the experimental system, was based on our
1660 g m− 3 in the experimental culture tanks. conclusion that the third tank can serve as a sedimen-
A dosing pump was adjusted to deliver the feeding tation and algae culturing unit at the same time. Total
suspension continuously to the culture tank (II) via 4 × 6 volume for this production unit was 10,000 l. The
mm polyethylene aquarium tubing (Fig. 1). feeding reservoir was a 400-l tank in which a daily dry
Except for the first two experimental trials (Table 1, diet ration was suspended, applying the same methods
A and B), when torula yeast was provided from the first described for the experimental system. Water flow in
day of culture, the mixture of dry diet suspension was this unit was 1500 l h− 1 in the initial days after stocking
delivered only at day 3 or 4, when the planktonic algal with Artemia nauplii and was gradually increased up to
population had been totally consumed by the growing 5000 l h− 1 during the five final days of the culture cycle.
early stages of Artemia.
Once a day the walls and bottoms of sedimentation 2.3. Experimental procedures
tanks (Tanks III) were brushed to suspend the sediment
and attached algae, and aeration was turned on for 4 h to Eight trials were carried out between September 2002
keep the microalgae in suspension, thus allowing them to and January 2003: Six trials in the experimental
flow to the subsequent tanks and prevent sedimentation production units and two in the pilot unit.
with development of anaerobic conditions and sulfides. In the experimental units, two trials (A and B) in
In the summertime, water loss due to evaporation September 2002 were conducted outdoors and four trials
(which was up to 3 cm day− 1; 350 cm annually; Zmora between November 2002 and January 2003 were carried
et al., 2002) was compensated by adding fresh tap water out in greenhouses.
(apart from the water in the feed). No water was In the pilot production units, the trials were done
discharged during the culture period. From May to outdoors during September and October 2002.
October, production units were outdoors, exposed to Experimental cycles were concluded when 25% of the
direct solar radiation. In this period, water temperature animals (assumed to be 50% of the females) developed
reached up to 32 °C in late afternoon. During the rest of detectable ovaries and reached a size of about 10 mm.
the year the working area was covered with a Temperature, oxygen and pH levels were monitored
polyethylene greenhouse and heaters kept the water twice daily at 08:00 and 14:00.
temperature at 25.5 ± 2.5 °C. Ammonia and total dissolved nitrogen levels (TDN)
were measured at the end of each experiment using a
2.2. The pilot production system Technikon Autoanalyzer II following the method
described in Krom et al. (1985).
The pilot production system was larger than the Three samples (250 ml each) were taken daily to
experimental system and based on its results. The first estimate the survival rate of Artemia. A 1-l sample was
tank was 2000 l in volume, the second one was a 3000- taken daily to estimate biomass. The sample was
l U-shaped trough, and the third was a 5000-l U-shaped strained through a sieve and the excess water was

Table 1
Average abiotic parameters in the culture tank (A, B — outdoor conditions; C, D, E, F — under greenhouse; to all the treatments we added 2 kg wet
weight or 0.4 kg DW Ulva lactuca at the start of the cycle)
Parameter A September B September C November D December E December F January Average S.D.
Temperature (°C) 08:00 24.46 ± 2.25 22.54 ± 3.36 24.77 ± 1.64 23.57 ± 3.18 23.82 ± 0.87
14:00 25.71 ± 1.79 24.95 ± 2.40 26.61 ± 1.16 24.69 ± 2.20 25.49 ± 0.74
Oxygen (mg/l) 08:00 5.38 ± 0.51 6.33 ± 0.86 5.89 ± 0.67 6.10 ± 0.77 5.93 ± 0.35
14:00 5.05 ± 0.37 6.16 ± 0.61 5.66 ± 0.54 5.91 ± 0.67 5.70 ± 0.41
pH 08:00 7.09 ± 0.02 7.10 ± 0.02 7.06 ± 0.02 7.07 ± 0.02 7.08 ± 0.02
14:00 8.11 ± 0.03 8.12 ± 0.03 8.04 ± 0.02 8.12 ± 0.01 8.10 ± 0.03
Final yield (kg/m3) 47.50 46.50 38.00 36.59 34.85 38.23 40.28 ± 4.89
Dry food (g) 9.10 9.10 5.88 6.48 6.93 6.76 7.38 ± 1.26
FCR (with Ulva) 0.20 0.20 0.17 0.19 0.21 0.19 0.19 ± 0/12
Survival (%) 22.98 33.88 15.50 26.12 24.62 ± 6.59
Final Artemia density 5.4 4.3 2.0 3.6 3.83 ± 1.23
(no./ml)
 O. Zmora, M. Shpigel / Aquaculture 255 (2006) 488–494 491

removed with blotting paper. This allowed us to 40.28 ± 4.89 kg m− 3 in the culturing tank (Table 1). The
approximately evaluate the total biomass of the culture culture from the September 2002 trials grew faster and
and estimate the food ration for the next 24 h. In addition reached maturity after only 17 days, and its final yield
to the dry feed, 10 kg (2 kg dry weight) of fresh was greater (47 kg m− 3). Average FCR was 0.19 ± 0.012
shredded U. lactuca was placed in the first tank at the (Table 1). Survival decreased gradually throughout the
start of each cycle. trials and averaged 24.62 ± 6.59% (Table 1, Fig. 3). The
At the end of the experiment, the total biomass in the final numbers of Artemia averaged 3.83 ± 1.23 indivi-
Artemia culture tank was weighed. A preliminary duals ml− 1, half of which were sexually mature adults
experiment had shown that a 1 L sample was represen- (∼ 10 mm long).
tative of the culture tank, and the values obtained on the Five to six days after the system was inoculated with
last day of culture matched the projected yield. Food microalgae (from 3 days before stocking the nauplii to
conversion ratio (FCR) was calculated as: 2–3 days after stocking) the planktonic microalgae
Food conversion ratio ðFCRÞ bloomed and reached a density of about 20 cm Secchi
disk. At the same time, a brown film of the benthic
¼ total feed intake ðg dry dietÞ
diatom N. cf lenzi covered the walls and bottoms of the
=total weight gain ðg wetÞ: tanks (Fig. 4A).
When nauplii became more efficient in their filter
The wet weight of Ulva was calculated as a dry feeding the planktonic microalgal population decreased
weight (20%) in the total feed intake. and benthic diatoms (N. cf lenzi) established significant
populations on the walls and bottoms of the tanks.
3. Results Microscopic observations revealed that diatom cells
used shredded Ulva as substrate; they covered the
3.1. Experimental production units numerous small pieces and also penetrated into the
thallus and propagated there rapidly (Fig. 4B and C);
Water temperature in the Artemia culture tanks was while some of the Ulva thallus kept growing, others
kept constant during the winter, averaging 23.80 ± 0.9 °C decomposed. Diatom cells flowed in significant numb-
at 08:00 and 25.50 ± 0.75 °C at 14:00. Oxygen levels ers to the Artemia culture tanks, settled and prospered in
were maintained via aeration at 90 ± 0.7% saturation the organic sediments, which were composed of
throughout the day. The pH levels averaged 7.08 ± 0.02 Artemia exoskeletons and fecal pellets in different
at 08:00 and 8.1 ± 0.03 at 14:00 (Table 1). Ammonia stages of decomposition, uneaten food particles, bacte-
accumulated during production and averaged at 4.67 ria, etc. (Fig. 4D).
± 2.1 mM l− 1 after 20 days. Maximal concentration When the aeration was turned off, the benthic diatoms
measured was 6.8 mM l− 1 (as Total Dissolved Nitrogen were undisturbed and renewed their biomass. This
— TDN) in the final days of culture. phenomenon was repeated daily. In the sedimentation
Starting as nauplii, Artemia grew to maturity in 19– tanks and the tanks with Ulva there were relatively dense
20 days (Fig. 2). The final biomass averaged (up to 1000 ind ml− 1) populations of the ciliate Euplotes

30
A Sep 02
25 B Sep 02
C Nov 02
20
Biomass (kg)

D Dec 02
E Dec 02
15
F Jan 03

10

0
Day 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

Fig. 2. Biomass accumulation in six 600-l tanks, in six replicates in the experimental unit (the two September 2002 experiments were done in outdoor
conditions and the other four replicates in greenhouses).
492 O. Zmora, M. Shpigel / Aquaculture 255 (2006) 488–494

120

100

80

Survival (%) 60

40

20

0
Day 7 8 9 10 11 12 13 14 15 16 17 18 19 20

Fig. 3. Survival rate (%± S.D.) of Artemia during 20 days of production (N = 6).

vannus. Apart from the very early stages, Artemia experimental units. Temperature measured in this system
apparently fed on this protozoan, because, although they ranged between 24 °C in the morning and 30 °C in the
were observed flowing into the Artemia culture tank, late afternoon. After 16 days of culture, total yield in two
virtually no ciliates were observed in the tank itself. This trials reached 93 kg, and cumulative diet was 21 kg,
supposition was confirmed in a laboratory scale excluding 2 kg DW of U. lactuca (Fig. 5). The average
experiment studying the capability of Artemia feeding yield of Artemia in the pilot system was 31 kg WW m− 3.
and growing on E. vannus and supported by microscopic Since we used 21 kg of dry diet, the FCR was 0.23 for dry
observations (results not shown). diet excluding the weight of Ulva, and 0.25 including it.

3.2. Pilot production unit 4. Discussion

Abiotic parameters as well as microalgae and ciliates The multi-step, intensive closed system described in
distribution were similar to those recorded in the this study integrates several ecological parameters to

Fig. 4. Diatoms found in the bottom of Artemia tanks (A), Navicula lenzi (B), and Navicula salinicola (C), on thallae of U. lactuca. N. lenzi on
Artemia feces (D) (EM photos were made by Prof. J.J. Lee from CUNY).
 O. Zmora, M. Shpigel / Aquaculture 255 (2006) 488–494 493

Artemia cultured in 3000 L tank

100
Biomass in Cycle 1
90
Biomass in Cycle 2
80 Diet in Cycle 1 (cumulative)
70 Diet in Cycle 2 (cumulative)
Biomass (kg) 60
50
40
30
20
10
0
Day 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16

Fig. 5. Biomass and feed accumulation of two replicates in 3000-l tank in the pilot unit (the experiments were done in outdoor conditions).

create the best conditions for the production of Artemia, a single long tank and most of the solid particles sank to
while taking advantage of inexpensive agro-techno the bottom of the first half of this tank. To simplify
products and photosynthesis. The different tanks in the culture methods and reduce costs, relatively long tanks
system, each with its own task, facilitate control of the may be applied in future production systems, as was
overall production. The first tank, containing the demonstrated in the pilot.
shredded Ulva, acted as an indirect food generator for The main difference between the system described in
the Artemia. The suspended detritus particles and this study and other production systems is in the
decaying Ulva provided a good substrate for the benthic approach to the waste products. Our system discharges
diatom cells, aerobic bacteria and grazing ciliates. The no waste products during the entire growth cycle,
150 μm filter on the outflow retained the large particles, whereas other intensive systems apply different methods
ensuring that they would continue to supply substrate for separating solid waste products (fecal pellets, etc.)
and nutrients from decay in the tank. and removing them. Any failure to do so leads to culture
The Artemia culture tank (II) kept the growing crash or poor results (Dhont and Lavens, 1996; Dhont
animals in a favorable environment which was and Van Stappen, 2003). Artemia survival in our system
provided with a constant flux of food, maintained a averaged 50% and 24% after 14 and 20 days
high level of DO, and allowed the dissolved (CO2, respectively and was similar to the mortality in other
ammonia) or suspended (fecal pellets, exoskeletons) described flow-through systems (Dhert et al., 1992).
waste products to be flushed out for utilization in the The relatively high pH during the day and the huge
succeeding tanks. gain in biomass, coupled with the extremely low FCR,
The solids evacuated from the culturing tank sank to indicate high photosynthetic activity. The mixed diet of
the bottom of the first sedimentation tank (III). There, diatoms, ciliates, yeast, and soy protein contributed to a
the sediment underwent decomposition by bacteria and much higher yield of Artemia biomass than in any other
was grazed by ciliates. Benthic diatoms may have taken culturing system so far described (15 and 25/kg/m3 for
up nutrients produced or released there, and were moved flow-through systems using micronised feeds and live
along to the next sediment tank while agitation was algae, respectively; Tobias et al., 1979; Dobbelier et al.,
occurring. 1980; Dhont and Lavens, 1996; Dhont and Van Stappen,
Tank IV was a diatom generator. It received a high 2003). In addition, the bacteria population which
concentration of dissolved nutrients and microalgae developed in the tanks might be an additional nutritious
(detached diatoms), and because it was exposed to direct source for the Artemia (Gorospe and Nakamura, 1996;
solar radiation during the day, the diatoms proliferated Milligan et al., 1980).
on its bottom, walls and central partition. Diatoms The system described in the pilot study was tested in
which had detached naturally or while the tank was a large tank at nearly industrial scale and its production
scrubbed and agitated, moved on to Tank I to enhance remained relatively high compared to other systems
the algae density (of the same species) there. In the pilot surveyed. Moreover, the FCR of our system was
unit, the tasks of Tanks III and IV were accomplished by extremely low (0.225), considering that an FCR of 3–
494 O. Zmora, M. Shpigel / Aquaculture 255 (2006) 488–494

7 in different temperatures in extensive systems Dhont, J., Van Stappen, G., 2003. Biology, tank production and
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Sorgeloos, pers. comm.). This fact would contribute Dobbelier, J., Adam, N., Bossuyt, E., Bruggeman, E., Sorgeloos, P.,
much to the cost effectiveness of the product at any 1980. New aspects of the use of inert diets for high density
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