Aquacultural Engineering 17 (1998) 215 239

The integrated culture of seaweed, abalone, fish and

clams in modular intensive land-based systems: II.
Performance and nitrogen partitioning within an abalone
(Haliotis tuberculata) and macroalgae culture system
Amir Neori a,*, Norman L.C. Ragg b, Muki Shpigel a
a

Israel Oceanographic and Limnological Research, National Center for Mariculture, P.O. Box 1212,
Eilat 88112, Israel
b
Department of Zoology, Uni6ersity of Canterbury, Pri6ate Bag 4800, Christchurch, New Zealand
Received 12 December 1996; accepted 7 September 1997

Abstract
A pilot-scale system for the intensive land-based culture of abalone was established using
an integrated design aimed at eliminating the dependence on external food sources, whilst
reducing water requirements and nutrient discharge levels. The system was the first and
simplest trial in a series of progressive complexity of the concept of integrated culture of
seaweed, abalone, fish and clams in modular and intensive land-based facilities. Relative sizes
of the modules, their stocking densities and the rate of nutrient supply were determined
based on earlier results to be optimal. Effluents from two abalone (Haliotis tuberculata)
culture tanks drained into macroalgae (Ul6a lactuca or Gracilaria conferta) culture and
biofilter tanks, where nitrogenous waste products contributed to the nutrition of the algae;
net algal production from each algal tank was harvested and used to provide a mixed diet for
the abalone. Excess algal yield was used elsewhere. The system was monitored to assess
productivity and nitrogen partitioning over a year, while improvements were made based on
the accumulating results. Total annual N-budgets were combined with mean production
figures to determine a suitable ratio of abalone biomass to algal culture vessel productivity,
towards commercial application of the concept. The abalone grew on average 0.26% and
0.25% body weight/d in the two culture tanks; reduced growth and increased food conversion
ratios (food eaten/biomass gain; w/w) were associated with high summer water temperatures
(max. 26.9C). U. lactuca showed reliable growth and filtration performance (mean production of 230 g fresh weight/m2/d, removing on average 58% of nitrogen supplied). Conversely,
G. conferta growth was highly erratic and was deemed unsuitable for the current application.

* Corresponding author. Tel: + 972 7 6361445/25; fax: +972 7 6375761; e-mail: neori@ocean.org.il
0144-8609/98/$19.00 1998 Elsevier Science B.V. All rights reserved.
PII S0144-8609(98)00017-X

216

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

It is estimated that 1 kg of abalone biomass would require food supplied by 0.3 m2 of U.

lactuca culture, reducing N inputs required by 20% and N in effluent by 34% when compared
to the two organisms grown in monoculture. 1998 Elsevier Science B.V. All rights
reserved.
Keywords: Seaweed; Abalone; Nitrogen recycling; Modular intensive land-based system

1. Introduction
Over exploitation by heavy artesanal fishing of the European abalone (or Ormer)
Haliotis tuberculata in the northern limits of its range, the British Channel Islands
and the French Brittany coast, and the subsequent depletion in natural stocks
during the second half of the twentieth century have resulted in increasingly strict
fishery legislation and reduced landings (Mgaya and Mercer, 1994). The continued
demand for abalone can not be met by the fishery. Therefore the feasibility of
culturing abalone has received some attention within the regions that previously
supported its main fisheries (Hayashi, 1982; Hahn, 1989; Mgaya, 1995). The high
value of H. tuberculata led to its introduction as a mariculture species into Ireland
in 1976 (Mgaya and Mercer, 1994), and in 1993 at land-based facilities of the Israeli
National Center for Mariculture (NCM), on the Gulf of Aqaba, Red Sea (Shpigel
and Neori, 1996; Shpigel et al., 1996).
The development of commercial abalone culture is frequently limited by the need
to acquire sufficient quantities of suitable dietary seaweed. Natural populations of
brown or red algae are usually required, which are often in short supply (Mercer et
al., 1993). However, large quantities of the ubiquitous chlorophyte Ul6a lactuca L.
can be produced in seaweed culture systems, which serve as biofilters and are
associated with intensive seawater fishponds (Neori et al., 1996). Ul6a sp. biofilters
have been successfully integrated into a number of other experimental and commercial mariculture systems, efficiently removing dissolved inorganic nitrogen from the
effluent water (Ryther et al., 1975; Tenore, 1976; Vandermeulen and Gordin, 1990;
Hirata and Kohirata, 1993). While reported as being effective in its application as
a biofilter, particularly in land-based systems, the produced biomass of Ul6a sp. has
been of limited commercial value (Kissil et al., 1992; Arieli et al., 1993). The
valuable rhodophyte Gracilaria sp. has also been cultured in mariculture biofilters
in Eilat and elsewhere (Ryther et al., 1975; Neori, 1991; Buschmann et al., 1994).
One proposed way of increasing the economic viability of seaweed biofilters has
been to feed the biomass produced to commercially valuable macroalgivores,
particularly abalone (Tenore, 1976). H. tuberculata was introduced for this purpose
in Eilat (Shpigel et al., 1996). Subsequent feeding trials revealed that H. tuberculata
displayed improved growth performance when fed a diet of Ul6a sp. supplemented
with Gracilaria conferta, compared to monospecific diets of either alga (Shpigel,
1995).
A novel bioengineering concept of a self-sustaining, self-cleaning, modular,
integrated, land-based abalone and seaweed culture unit was first outlined by

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

217

Shpigel and Neori (1996), as the simplest of several combinations of progressive

complexity. The proposed pilot-scale, two-organism, abalone-seaweed system was
subsequently constructed at the NCM as a first step toward ultimately developing
a polyculture system for four organisms (seaweed, abalone, fish and clams). The
performance of the simple two-organism system, with regard to abalone growth
parameters and nutrient regimes, is described in the present report.
Inorganic nitrogen is the main nutrient that, when added to pristine coastal seas,
causes marine eutrophication (McCarthy, 1980). Furthermore, the most costly
component of diets used in aquaculture is protein, which also is a major determinant of the nutritional value in diets of the abalone H. tuberculata (Mai et al.,
1994). Recycling of nitrogen and reduction of its release to the environment are
major anticipated benefits of the proposed polyculture concept. N-budget was,
therefore, selected as the optimal measurement criterion for this aspect of the
experimental system.

2. Materials and methods

2.1. Organisms
Haliotis tuberculata were introduced into land-based facilities at the NCM from
Guernsey, UK, in 1993 (Shpigel et al., 1996). Ul6a lactuca L. was produced from
vegetative thalli isolated from the Red Sea and cultured in biofilters (Vandermeulen
and Gordin, 1990). Gracilaria conferta cultured in the second biofilter had been
collected on the Mediterranean coast of Israel (Levy and Friedlander, 1990).

2.2. System design

A two-organism (seaweed and abalone) culture system was built as diagrammed
in Shpigel and Neori (1996). The experimental system was designed to allow an
evaluation of the biological-chemical practicality of the abalone-seaweed integrated
culture concept, not specifically to maximize performance. Therefore, a large
margin of error was allowed, by using low stocking densities of the animals and
relatively large seaweed biofilters. The sizes of the abalone and the seaweed culture
vessels were adjusted with the following considerations:
1. A low abalone density (far below the 35 kg/m3 found practical in our regular
abalone culture systems);
2. Maximal consumption of seaweed expected, with a food conversion ratio
(FCR) of 25 kg fresh seaweed per 1 kg of abalone growth (Shpigel et al., 1996);
3. Minimal seaweed productivity expected (only 0.5 kg fresh weight m 2 week 1;
Friedlander et al., 1987, 1991; Neori, 1991; Neori et al., 1991, 1996).
Abalone were cultured in two similar bottom-draining square 600-l PVC tanks
(labelled A and B) of 1.0-m side length. The tanks were elevated, allowing their
effluents to drain into the seaweed biofilters described below. A removable screen
(1-cm mesh) covered the whole area 10 cm above the flat bottom, and retained the

218

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

abalone while allowing faeces and detritus to drain from the tank; water was
drained via a removable, 40-mm ID, 60-cm tall stand-pipe, fitted to a hole at the
bottom and covered by a 5-mm mesh at the top. Two perforated horizontal
aeration tubes on the bottom below the screen kept food algae in suspension. Eight
160-mm diameter PVC half-pipes were stacked on the screen and provided,
combined with the tank walls, approximately 5.2 m2 of wet surface area available
for abalone attachment. The abalone tanks were each initially stocked with 235 H.
tuberculata of 30 60-mm shell length (4.132.6 g wet weight) with a total biomass
of 2.2 kg (Table 1).
Two seaweed biofilters, identical to those reported in Neori et al., (1996), were
installed, one stocked with U. lactuca and the other with G. conferta. They were
made of round-bottom elongated (3 1.1 m) fiberglass tanks, bottom-aerated and
with a useable water volume of approximately 1500 l. U. lactuca and G. conferta
were stocked at 1.5 kg and 12.0 kg m 2 (fresh weight) respectively, following the
recommendations of Neori (1991) and Neori et al. (1991). The only nutrient source
for the whole system was mineral fertilizer (solutions of ammonium sulfate and
disodium phosphate), supplied directly to both biofilters by continuous dripping.
The N supply rate was initially about 5.6 g N m 2 day 1. This ammonia-N flux
was estimated to provide an optimal combination of good seaweed growth, about
50% removal of ammonia-N and a moderate N-content in the seaweed (Cohen and
Neori, 1991; Neori et al., 1991). From July 1995 onward ammonia-N was supplied
to the seaweed at only about 4.0 g m 2 day 1, in an effort to improve the fraction
of N removed by the biofilters. The influx of orthophosphate was maintained
throughout the year at 0.6 g P m 2 day 1. In addition, the U. lactuca biofilter
received the entire effluents from abalone tank A and the G. conferta biofilter from
abalone tank B.

2.3. System monitoring

The integrated culture system was monitored for 1 year, beginning in March
1995.

2.3.1. Abalone
At the time of initial stocking, seventy-five animals in each tank were randomly
tagged. They were wet weighed (after inverting each animal on absorbent paper to
remove excess water from the mantle cavity) and shell length measured at 23month intervals. Length is not a particularly useful growth parameter in abalone. It
was measured and presented below only to allow the readers comparison with
previous studies were weight was not used. The tagged abalone were assumed to
constitute a sub-sample representative of the tank population. Wet weight figures
were used to calculate for each time interval specific growth rates (SGR%; Eq. (1)),
the percent body weight gain per day (Shpigel et al., 1996).
SGR% = 100 ([ ln {Wt} ln {W0}]/t)

(1)

May 1995
100
0.47

286

392

April 1995
235
2.30

4.62

1067

2.67

787

Animals were added before sampling dates.

Abalone
restocking
Date
Individuals
Kilograms

Abalone
Standing
stock (kg)
Growth (mg
N/tank/d)

Water flow
rate (l h1)

January 1996

March 1996

June 1995
80
0.93

170

5.16

833

October 1995
591
4.52

517

8.34

510

332

8.96

525

April 1995
235
2.19

150

2.28

520

April 1995

August 1995

April 1995

June 1995

Tank B

Tank A

Sampling date

Table 1
Basic information on the abalone culture tanks and seaweed fresh-weight yield in two biofilter tanks

May 1995
100
0.48

203

4.06

1075

June 1995

June 1995
80
0.77

315

8.5

531

January 1996

October 1995
276
2.17

552

8.91

508

March 1996

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

219

220

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

where W0 is the wet weight of an animal at the beginning of each monitoring

interval and Wt is the weight after t days of growth, at the end of the interval.
The mean daily net biomass gain of the abalone (DB) in each tank was estimated
for each day of intensive sampling by Eq. (2).
DB =(B0 SGR%/100) Mw

(g/d, fw)

(2)

Where B0 is total biomass at the start of the day and Mw the weight of dead
animals removed (dead animals were removed on a weekly basis and their shell
lengths used to predict equivalent live weight using linear regression equations fitted
to the loge length:loge weight relationship in the tagged animals). On three occasions during the observation period (in May, June and October 1995), based on the
observation that U. lactuca production (Table 2) by far exceeded consumption by
the existing stock, and to offset the mortalities, additional abalone were stocked
(Table 1); B0 was corrected accordingly.

2.3.2. Algal production and abalone feeding

Abalone in both tanks were fed a mixture of fresh seaweed from the biofilters of
both systems. The seaweed was fed to the abalone in considerable excess (12 times
the weight of corresponding abalone biomass, maintained by supplying additional
seaweed every 2 3 d), to provide good shade for the animals as well as to ensure
that food was continuously available. The experiment was interrupted for 2 months
following the November 22nd 1995 earthquake in the Gulf of Aqaba; however, the
animals were fed seaweed from other tanks and the monitoring of the animals
continued.
Table 2
Seaweed fresh-weight yield (g/m2/d) in two biofilter tanks in 1995 and 1996
Date

Ul6a lactuca

Gracilaria conferta

Late April 1995

Early May 1995
May-June 1995
Late June 1995
Early June late July 1995
Early July 1995
Late July 1995
Late August 1995
September-October 1995
Late October 1995
October-November 1995
Mid-November 1995
Mid-January 1996
Late January 1996
Early February 1996
February-March 1996
Mid-March 1996
Late March 1996

210
403
286
412

194
295
303
284
196
155
168
81
52
104
85
95
402

46
261
268

170

57
34

14
330
39
11
197
136

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

221

Biofilters were drained every 2 weeks, the seaweed weighed and re-stocked at the
original weight. The net yield of algae, including weight of algae harvested for
feeding, was used to calculate the mean daily seaweed production for each 2-week
period.
The abalone tanks were drained weekly by removing the stand pipe; the debris
(assessed visually to be of negligible quantity) that settled to the space between the
bottom and the screen above was flushed and cleaned from the bottom; dead
animals were removed and their shell length measured; uneaten algae were removed
and weighed; the quantity of algae ingested was determined by difference from the
total weight fed.
Ingestion rate was estimated by dividing the seaweed weight, ingested during the
time interval between two weighings, and the mean abalone biomass for that
interval (estimated using SGR% and initial abalone biomass measurements for that
interval).
Food conversion ratio (FCR) was determined by the fresh weight of ingested
seaweed divided by the abalone biomass gain over the same time interval. Algal
growth inside the abalone tanks, and consequent possible nutrient recycling in situ,
was not assessed, hence the estimates of ingestion rate and food conversion ratio
are considered apparent.
Annual values of SGR% and FCR were calculated by the sums of ingested
seaweed and abalone growth, adjusted for mortalities and animal stocking.

2.3.3. Nutrient analyses

Sixteen individuals of H. tuberculata grown under conditions similar to those
described above were sampled at 3-month intervals during 1994; individual wet
weight was measured, the animals were then rinsed in fresh water and freeze-dried.
Each dry abalone was homogenized in a mill and its total nitrogen content was
determined by the Kjeldahl method. Fifteen samples of both seaweed species were
taken between April 1994 and April 1996 and treated in the same way as the
abalone samples. The mean nitrogen content of the animals and DB were used to
estimate the amount of nitrogen incorporated into abalone tissue during any
specific 24-h period. Similarly, nitrogen incorporation into algal tissue was determined as the mean tissue nitrogen content mean daily production.
The form, quantity and diurnal fluctuation of nitrogen and phosphorous flowing
into and out of each tank were determined at approximately 2-month intervals by
intensive sampling days from one morning (08:30) to the next (P was analyzed in
only about half of the days). Each such day was divided to four 6-h sampling
periods. Each water sample from a tank was collected during the entire 6-h period
in a separate covered 20-l PVC container via a drip siphon from the effluent
stand-pipe. The collected water, typically 5 l, was sub-sampled for analysis. All
sampling and storage vessels for the sampling were pre-soaked for 24 h in 1.0 N
HCl and then rinsed well with de-ionized water.
Total nitrogen (TN) and total phosphorous (TP) were analyzed by a Technicon
Autoanalyzer II using standard methods and following the modified persulphate
oxidation procedure as described by Neori et al. (1996). Total dissolved nitrogen

222

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

and phosphorous (TDN and TDP) were analyzed similarly, only following filtration
through acid-washed Whatman GF/C filters. Sub-samples of these filtrates were
deep-frozen, for subsequent determination of the mineral forms of N (DIN) and P
by standard Autoanalyzer methods (Krom et al., 1985). Suspended particulate
nitrogen (PN) was determined by the difference between TN and TDN, and
dissolved organic nitrogen (DON) was estimated by subtracting DIN from TDN.
Flowmeter readings were used to determine mean flow rate of water through the
tanks during each sample day (Table 1). Water flow and nutrient concentration
were used to determine the overall rate of input and output of nutrients for each
tank and biofilter. Net abalone production of N and P and their net uptake by the
biofilters were calculated as the difference between absolute levels entering and
leaving each tank.
Complete system nitrogen budgets were constructed for each 24-h sampling
period with the absolute nitrogen quantities, according to the scheme in Fig. 1.
Nitrogen partitioning was also standardized by biofilter water surface area or
abalone biomass to give comparable nitrogen budgets for the biofilters and abalone
tanks separately.

3. Results

3.1. Temperature
The greatest diurnal variations experienced by the abalone, up to 5.5C, occurred
during the spring (Fig. 2). Annual temperature extremes were 16.0C and 26.9C.
The algal biofilters, being downstream and with a longer residence time, experienced larger diurnal temperature variations all year round.

3.2. Abalone performance

Initial abalone growth rates differed between the two tanks, but converged
during April May 1995 to subsequently follow similar patterns. The best growth
(both SGR% and shell length) occurred in the spring, and it progressively declined
towards an autumn minimum (Fig. 3). By February 1996 growth rate had begun to
increase. Over 1 year, the tagged animals grew with an average SGR% of 0.262 9
0.033%/d (n =28) in tank A and 0.2519 0.037%/d (n= 31) in tank B.
FCR values (Fig. 4) were low (i.e. efficient) and relatively stable during the
spring, but increased (i.e. became less efficient) in summer to maxima in October of
4093.3 in tank A and 29 92.5 in tank B. Annual FCRs of 20 and 17 were
calculated for the two abalone tanks, using the overall growth (corrected for
mortalities and animal restocking) and seaweed ingestion values.
Abalone mortality (Fig. 5) was high following initial stocking of the systems,
with up to 13.6% of the animals dying within 1 month. Subsequent mortality
decreased during the summer and rose in autumn 1995 and again in spring 1996.
Cumulative annual mortality was 32.8% and 39.6% in tanks A and B, respectively.

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

223

Fig. 1. Schematic partitioning of nitrogen within an integrated abalone/algal biofilter culture system.
Dotted arrows represent recycling of nitrogen within the system.

224

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

Fig. 2. Daily variation between minimum and maximum water temperatures measured over a year in
abalone culture vessels and seaweed biofilters.

However, the interpretability of these annual figures in relation to Fig. 5 is

compromised by the periodic restocking of the tanks, as reported in Table 1. The
high mortality rates in the early months are offset in the overall annual rate by the
larger animal numbers later. The dead animals were generally found in areas where
the abalone tended to crowd, notably in the darkest corners of the tank; aggressive
behaviour, the use of the radula to inflict foot lesions on conspecifics, was observed
within these stacks.

3.3. Algal production

Production of Ul6a lactuca was seasonally-dependent (Table 2). Production was
lower in winter than in the rest of the year, averaging 2929 5 g fresh weight m 2
d 1 (529 1 g dry weight m 2 d 1) in the summer, and 839 9 g fresh weight m 2
d 1 (159 1 g dry weight m 2 d 1) in winter. Production rates in the spring and
autumn showed greater variability; annual maximum and minimum values of 412 g
fresh weight m 2 d 1 and 52 g fresh weight m 2 d 1 were recorded. Gracilaria
conferta yield was erratic and consistently lower than U. lactuca (Table 2). Algal
stocks within the G. conferta biofilter repeatedly crashed during the monitoring
period. A cessation in net growth was followed by frond fragmentation and
washout, and then a take over by opportunistic chlorophytes, predominantly Ul6a
spp. and Enteromorpha spp (see also in Friedlander et al., 1987, 1991; Ugarte and
Santelices, 1992; Buschmann et al., 1994). When production could be sustained, in
AprilJune 1995, it averaged 231931 g fresh weight m 2 d 1.

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

225

Neither seaweed tank functioned following the strong Gulf of Aqaba earthquake
of 22 November 1995, until January 1996; subsequent G. conferta production was
too low and erratic to permit harvesting and feeding to the abalone, and therefore
the abalone did not receive this algae in 1996 (see Table 3).

3.4. Nitrogen partitioning

3.4.1. Abalone tanks
Mean N content of abalone was 1.64 9 0.07% of wet weight (12.029 0.09% of
soft tissue dry weight), in U. lactuca 0.8190.05% of wet tissue (4.69 0.1% of dry
weight) and in G. conferta 0.81 9 0.06% in wet tissue (5.89 0.26% of dry weight).
These values were used to calculate budgets in N units (Table 3).
The significant inputs of N to the abalone tanks were abalone protein (taken into
account in the abalone growth figures) and seaweed protein. Each abalone tank
received seaweed biomass from the biofilters downstream. Overall, the A abalone
tank received from 58% to 100% of its seaweed N as U. lactuca and the rest as G.
conferta, and the B tank received from 64% to 100% of its N as U. lactuca and the
rest as G. conferta (Table 3).

Fig. 3. (a) Mean specific growth rates (SGR) and (b) mean daily shell length growth increments (9S.E.)
of samples of 75 tagged H. tuberculata grown in vessels A and B.

0
356
70
150
30
506
100
147
29
249
49
396
78
110
22
392
1351

N Outputs
Abalone growth
% of input total
Effluents
% of input total
N output total
% of input total
Deficit (out-in)
% of input total
Abalone growth
Total, mg N/tank
Seaweed input
Total, mg N/tank

April 1995

N Inputs
Inflowing water
Ul6a lactuca
% of input total
Gracilaria conferta
% of input total
N input total
% of input total

Date:

Tank A

3119

286

59
9

62
9
554
82
616
91

0
394
58
281
42
675
100

June 1995

2508

170

251
52

33
7
202
42
235
48

0
310
64
176
36
486
100

August 1995

2043

517

4
2

62
25
187
76
249
102

0
245
100
0
0
245
100

January 1996

4803

332

76
14

37
7
423
79
460
86

0
536
100
0
0
536
100

March 1996

1379

150

392
65

66
11
147
24
213
35

0
430
71
175
29
605
100

April 1995

Tank B

2509

203

427
69

50
8
141
23
191
31

0
394
64
224
36
618
100

June 1995

2010

315

74
31

37
16
125
53
162
69

0
237
100
0
0
237
100

January 1996

4776

avg.
552

54
10

62
12
528
99
590
110

0
536
100
0
0
536
100

March 1996

24 498

2918

62
14
284
59
346
72

0
382
81
112
19
494
100

2722

sum
324

148
28

Average SD

1222

135

161
27

32
8
161
25
165
27

103
18
106
18
146
0

Table 3
Daily N budgets for abalone tanks A and B on dates of intensive sampling during 19951996. Figures represent biomass-specific rates (microgram N/g abalone /d), and the corresponding percentages relative
to the total N input to the tank

226
A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

227

Fig. 4. (a) Mean ingestion rates and (b) calculated food conversion ratios (FCR, fresh weight of algae
ingested/abalone weight increase) of H. tuberculata grown in vessels A and B. Symbols as in Fig. 3.

The nitrogen leaving in the effluents of the abalone tanks originated from feeding
activity of the animals (metabolic by-products, undigested material and algal cell
contents not ingested), as negligible quantities of N came in with the fresh seawater
(Table 3). The nitrogen supplied as seaweed protein was either incorporated into
abalone biomass, washed out of the abalone tank into the biofilter or was
unaccounted for (deficit). During most of the days monitored, much of the N
entering the abalone tanks (up to 69%) remained unaccounted for, whereas on two
occasions N surpluses of 2% and 10% were measured (Table 3). On average, of the
N that entered the abalone tanks only 149 8% was incorporated into abalone
biomass over the entire monitoring period. Of the rest of the N that entered the
abalone tanks, 59 9 25% flowed out into the seaweed biofilters with the effluent and
28927% was not found (Table 3).
Total N in the abalone effluents averaged for the entire nine intensive sampling
data sets (five for tank A and four for tank B) was 3019 73 mg N/g abalone/d
(Tables 3 and 4). This TN value was comprised of ammonia-N (629 12 mg N/g
abalone/d), DON (145 9 63 mg N/g abalone/d), and PN (101 9 55 mg N/g abalone/
d). The production rate of TN and its components did not show discernible

228

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

Fig. 5. Monthly abalone mortality, expressed as a percentage of the standing stock present at the
beginning of each month, in abalone culture vessels A and B.

significant diurnal patterns (Table 4). Oxidized nitrogen was not detected in any of
the samples from tanks A and B, suggesting that either nitrification did not occur
there or that the nitrification was tightly coupled with denitrification, which
consumed all the oxidized N.

3.4.2. Seaweed biofilters

Smaller fractions of the N supplied to the seaweed exited the biofilters in the
effluents in summer than in winter (Table 5). U. lactuca, on 3 out of 4 days
monitored, incorporated larger fractions of the N entering the biofilter into seaweed
Table 4
Quantity and forms of nitrogen production measured in abalone tank effluent water during 6 h
sections of 24 h monitoring periods; figures represent mean microgram N/g abalone biomass, produced
during 6 h (9 S.E.; 5 dates in tank A and 4 dates in tank B)
Form of N in abalone
effluent:

Ammonia-N
Dissolved organic N
Particulate N
Total N

Sample period:
08:3014:30

14:30 20:30

20:30 02:30

02:30 08:30

18 ( 911)
38 (946)
9.3 (915)
64 (9 38)

11
52
31
91

19
26
23
65

14
26
37
78

(911)
(9101)
(9 51)
(9 97)

(914)
( 944)
(9 26)
(949)

( 911)
( 927)
( 986)
( 983)

Total/d
62 (912)
145 (9 63)
101 (9 55)
301 (9 73)

1059
18

Deficit (out-in)
% of input total
47

1687
29
3107
53
4794
82

Outputs
Algal harvest
% of input total
Effluents
% of input total
N-output Total
% of input total

Filtration efficiency
in biofilters (%
of input total)

221
4
5632
96
5853
100

Inputs
From abalone tank
% of input total
Added nutrients
% of input total
N-input-total
% of input total

59

496
8

3316
52
2619
41
5935
92

853
13
5578
87
6431
100

66

444
10

2437
56
1505
34
3942
90

348
8
4038
92
4386
100

42

1075
24

834
18
2649
58
3483
76

520
11
4038
89
4558
100

Date: April 1995 June 1995 August 1995 January 1996

Ul6a

42

979
18

3231
61
3049
58
6280
118

1263
24
4038
76
5301
100

76

4243
74

130
2
1370
24
1500
26

111
2
5632
98
5743
100

88

3718
64

1365
24
686
12
2051
36

191
3
5578
97
5769
100

29

316
7

1587
36
3122
71
4709
107

355
8
4038
92
4393
100

187
3

0
0
5419
97
5419
97

1568
28
4038
72
5606
100

March 1996 April 1995 June 1995 January 1996 March 1996

Gracilaria

Table 5
Daily N budgets for biofilter tanks stocked with Ul6a lactuca and Gracilaria conferta on dates of intensive sampling during 19951996. Figures represent
for each tank area-specific rates (mg N/m2 of biofilter tank/d), and the corresponding percentages relative to the total N input to the tank
A. Neori et al. / Aquacultural Engineering 17 (1998) 215239
229

230

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

Table 6
Overall N budget for the integrated culture system (two abalone vessels and two seaweed biofilters).
Annual averages, calculated from Tables 2 and 4
mgN/m2/d
Input

SE

% of N input

4734

779

105

44

Seaweed
Total harvest
Fed to animals within the system
Unused (export)

1621
878
743

1139
394

34
19
16

Effluents

2614

1293

55

Outputs
Abalone growth

Deficit (out-in)

1273

100
2.2

27

production than did G. conferta (Table 5). Overall, nitrogen filtration efficiency of
the biofilters was highest in summer (Table 5). Although the G. conferta biofilter
occasionally removed N more efficiently than the U. lactuca biofilter, it incorporated a smaller fraction of N into a harvestable biomass and created larger
N-deficits. Generally, the U. lactuca tank removed 58% of the N input to the
system, while its total harvest contained about half the average inorganic N input.
The algal harvest from the G. conferta tank contained only about a quarter of
inorganic N that supplied large fractions of unaccounted-for N were associated
with visual observations of frond fragmentation in this seaweed.
Most of the N budget was comprised of ammonia, the inorganic form supplied
to the biofilters, and the other N forms were inconsequential. DON and PN (data
not shown) were sometimes removed and sometimes produced in the biofilters, but
in small quantities (B 10% of the overall N budget). Oxidized N (data not shown)
was sporadically produced in both biofilters in small quantities (up to 5% of the
overall N budget).

3.4.3. O6erall N budgets

In the overall N budget of the abalone tanks and their seaweed biofilter tanks
(Table 6), the seaweed harvest contained about one third of the total N input.
However, only about half of this harvest was fed to the animals. These assimilated
about 12% of the seaweed given to them, and therefore only 2.2% of the total N
supplied was harvested as abalone biomass.
There was, however, a large net seaweed surplus, about half of the overall
production of algae in both biofilters. Nearly twice as much surplus was produced
by U. lactuca than by G. conferta. About half of the N input of the entire four-tank
system was released in the effluents, and about a quarter of the N was unaccounted
for (deficit). The deficit N (which possibly was also released) within G. conferta
biofilter was greater than in the U. lactuca biofilter.

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

231

3.4.4. Phosphorous
No phosphorous was detected in the influent or effluent water of either abalone
tank. The biofilters (data not shown) both consistently removed less than 25% of
the phosphorous added (with the exception of the G. conferta in January 1996, that
removed 84.8% of phosphorous encountered over 24 h).

4. Discussion
The concept of ecological sustainability in aquaculture refers to the maximization
of internal feedback (e.g., recycling) within a culture system. This minimizes the
inputs and the wasted outputs of resources (Dalsgaard et al., 1995), such as
nutrients, water and energy, in effluent water. The results presented here show the
potential of the integrated abalone-seaweed culture to be practical. A quantitative
evaluation of the performance of each component of the system studied here will
aid in the development and design of more practical facilities and techniques for
integrated mariculture, based on internal nutrient recycling and leading to better
effluent quality. The system incorporates a number of features that can increase the
ecological sustainability of the proposed integrated culture system, as follows: (a)
the use of the same water for both abalone and seaweed cultures reduces seawater
requirements by half in this first trial; (b) biofiltration and recycling of the abalone
nutrient excretions by the seaweed reduces both the nutrient input requirements and
the overall environmental impact of the culture operation; (c) the use of biofiltergrown seaweed eliminates the need for a destructive harvest of natural seaweed
beds; and (d) the chemical composition of the cultured seaweed, and hence their
nutritional value to the algivores, is controllable.
Following refinements to the integrated culture system that can arise from the
present results, the incorporation of fish and bivalves will follow, according to the
principles of the more complex designs proposed and outlined by Shpigel and Neori
(1996).

4.1. Abalone performance

Best H. tuberculata performance was seen in spring (MarchMay), when water
temperatures corresponded closely to the summer temperatures considered optimal
for growth in the Ormers natural range (Hayashi, 1982; Clavier and Richard,
1986). The initial differences observed in SGR% between the two abalone populations may be explained by differences in the timing of spawning, usually synchronous within a confined abalone population (A. Marshall, NCM, Israel,
personal communication).
From May to October, when daytime water temperatures in Eilat remained
above 23.5C, growth rates of the Ormer were low, reflected by increased FCRs. It
has been suggested (Shpigel et al., 1996) that the elevated temperatures increase
basal metabolic rate, thus reducing the energy available for somatic growth.

232

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

Ingestion rates remained fairly constant throughout the year, in close agreement
with rates recorded by Mercer et al. (1993). They reported 59% daily body weight
food ingestion by H. tuberculata fed U. lactuca, suggesting that the animals in the
present study were feeding to satiation.
Overall growth performance, expressed as annual shell length growth increment,
was inferior in the present study when compared to values previously reported in
Eilat (Shpigel et al., 1996). Elsewhere, for H. tuberculata of similar size ranges
grown in warm water culture (18 20.5C), growth rates of 1520.3 mm year 1
were recorded (Forster, 1967; Hayashi, 1980, 1982; Mgaya and Mercer, 1995). In a
parallel experiment H. tuberculata from the same stock as used in the present study
showed growth rates corresponding to 21.8 9 2.7 mm year 1, in a controlled
aquarium environment (Ragg et al., unpublished data). In the present study
abalone were stocked at densities (maximum 166 individuals m 2) well below the
levels that were suggested by Koike et al. (1979), and by Mgaya and Mercer (1995)
as causing significant crowding pressure. However, the tank design in the present
study allowed animals to move freely, hence the abalone, responding to the same
stimuli, such as negative phototaxis (Mgaya and Mercer, 1994), and their gregarious nature (Douros, 1987) tended to crowd. This apparently induced local effects of
severe crowding pressure, smothering and cannibalism (unpublished observation)
and resource competition that is likely to interfere with growth (Koike et al., 1979;
Mgaya and Mercer, 1995). Despite an apparently considerable scope for improving
growth performance, mean annual SGR%s and FCRs were better here than the
conservative estimates proposed by Shpigel and Neori (1996) (Table 7) and
concurred with those found by Mercer et al. (1993).
Smothering and aggressive behaviour between conspecifics are held partly responsible for observed abalone mortality, and initial high mortality is likely to be
associated with handling stress incurred during stocking (Mgaya and Mercer, 1995),
and high autumn mortality is attributed to the rapid decline in water temperature
(Aviles and Shepherd, 1996).

4.2. Algal production

Algal biomass production in the U. lactuca biofilter was highly seasonal, the
growth rate of U. lactuca appearing to be predominantly dependent upon water
temperature and light, in agreement with the findings of Vandermeulen and Gordin
(1990), Israel et al. (1995) and Neori et al. (1996). Constant daily yields accompanied the more stable water temperatures during winter and mid-summer, with
production levels comparable to those of U. lactuca grown in other biofilters (Neori
et al., 1991, 1996) and using artificial inorganic nitrogen and phosphorous sources
(DeBusk et al., 1986; Israel et al., 1995). The annual mean seaweed production of
230 g fresh weight (42 g dw) m 2 d 1 obtained here exceeds that of almost all
known intensive terrestrial and marine plant cultures (Lapointe et al., 1976).
Gracilaria spp. is highly sensitive to temperature (Edding et al., 1987; Friedlander
et al., 1987, 1991; Levy and Friedlander, 1990; Ugarte and Santelices, 1992);
optimum growth of G. conferta occurs in cultures of 2026C (Levy and Friedlan-

Yield of Ul6a lactuca (kg

fresh weight d1)/kg N
added to system
Biofilter surface area required
to support this production
Yield of abalone (kg fresh
weight d1)/kg N added to
system
Volume of water required to
support this production of
abalone
25 m3

2.6

250 m2

65

Predicted by Shpigel
and Neori (1996)

SGR = 0.3% d1; stocked at

35 kg m3

25.7 m3

SGR= 0.3% d1; stocked at

35 kg m3

Receives a net N-flux of 4 g

m2 d1; yield 0.23 kg m2
d1
U. lactuca yield of 0.23 kg m
2 d1
FCR= 20

Calculated from mean values Assumptions

found in the present study

Removes 55% of ammonia-N 54.9

at flux of 4 g m2 d1; yield
0.25 kg m2 d1
U. lactuca yield of 0.25 kg
239 m2
m2 d1
FCR=25
2.7

Assumptions

Table 7
Comparison between the yields, and corresponding system dimensions, predicted for an integrated H. tuberculata/U. lactuca system per kg of nitrogen
input, using the figures proposed by Shpigel and Neori (1996) and the mean annual yields found possible in the present study

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

233

234

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

der, 1990) supplemented with nutrients in a single weekly pulse (Friedlander et al.,
1991; Levy and Friedlander, 1994). It is therefore suggested that stress imposed by
summer and winter temperature extremes, as well as large diurnal ranges, combined
with the continuous presence of nutrients, favouring the development of fouling
chlorophytes, were responsible for the poor performance of G. conferta in the
present study.

4.3. Nutrient partitioning

4.3.1. Abalone tanks
On an annual average, dissolved N formed about two-thirds of the total N
excretions in the abalone tanks (disregarding the N deficit). This value is exactly as
we had reported for marine fish in intensive fishponds (Krom and Neori, 1989) and
integrated fish-seaweed ponds (Neori et al., 1996), and with about similar deficits.
In most of the nitrogen budgets of the abalone vessels presented here a large
proportion of the nitrogen remained unaccounted for. These deficits are attributed
to several possible sources of inaccuracy:
1. Analytical errors in determining the volumes of water (estimated at  10%);
2. Budgets were constructed for specific 24-h periods, while considerable day-today variability may exist;
3. Macroalgae show variable levels of tissue nitrogen, depending on ambient
conditions, particularly the level of dissolved inorganic nitrogen in the water, and
also light and temperature (Friedlander et al., 1987; Vandermeulen and Gordin,
1990; Cohen and Neori, 1991; Pedersen, 1994). In the present study, average values
were used to represent the nitrogen content of either algal species throughout the
monitoring period, hence no accommodation was made for possible variations in
the amount of nitrogen within food algae or the subsequent uptake or loss of
nitrogen by the algae within the abalone vessels.
4. Tightly-coupled nitrification-denitrification in animal digestive tract, faeces or
in corners of the rectangular vessels. Such efficient coupling that leads to the
complete removal of the oxidized N as soon as it is produced has been known for
highly organic flooded soils and sediments (Reddy and Patrick, 1984). It could
explain both the absolute lack of oxidized N in the abalone tanks (as opposed to
its sporadic detection in the waters of the seaweed tanks) and the large N-deficit
there.
5. Fouling organisms growth on the solid surfaces and on the shells.
6. Solid waste drained only during routine maintenance and evaluated visually to
be negligible.
Microorganisms probably could not substantially affect the nitrogen budget of
the abalone tanks. Vigorous aeration and bottom-draining prevented the formation
of dead spaces, where organic matter and bacteria could accumulate (Dvir, 1995),
and abalone grazing kept all hard surfaces visibly free of fouling. It is possible that
the amount of nutrients lost during the weekly cleaning of the tanks was much
more than we assessed.

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

235

Diurnal variation in composition of nitrogenous abalone effluent was on average

limited to ammonia, most probably a net result of periods of greatest abalone
activity (Barkai and Griffiths, 1987; Peck et al., 1987; Fleming et al., 1996) on the
one hand, and daylight uptake of ammonia by the uneaten seaweed (Cohen and
Neori, 1991) on the other hand. Un-ingested algal cell contents liberated by abalone
radula scraping action may account for the persistently high presence of DON and
PN in tank effluents. Average ammonia production rate of 62 mg N/live g/d in the
present study appear higher than the 36 mg N/live g/d, which can be calculated for
a 9.3-g (4 g dw) animal by the equation given in Peck et al. (1987):
ln U =0.656 ln W 0.914

(3)

U = ammonia excretion in mmol N/h and W= dw of whole animal. This is not

surprising, considering the markedly higher temperatures in our study.

4.3.2. Seaweed biofilters

The U. lactuca biofilter showed consistent performance throughout the year and
most of the nitrogen removed in this biofilter was accounted for by subsequent
gains in algal biomass. Biofiltration efficiency was highest in summer, corresponding to fastest U. lactuca growth. The filter removed approximately half of the
nitrogen, encountered predominantly as ammonia-N, at an even rate over 24 h, as
noted by Vandermeulen and Gordin (1990) and by Cohen and Neori (1991). The
consistent biofiltration performance of U. lactuca is highlighted when comparing
the present nitrogen removal efficiencies to those recorded by Cohen and Neori
(1991) who, working at the same site, found mean removal rates of 4956% of
ammonia-N supplied at fluxes of 4.8 5.2 g m 2 d 1. Cohen and Neori (1991) also
demonstrated that nitrogen filtration efficiency was enhanced as influent nitrogen
flux decreased; however, there was a corresponding reduction in U. lactuca tissue
nitrogen, which has been shown to reduce the dietary value for H. tuberculata
(Ragg et al., unpublished data).
The low removal efficiency of phosphorous in the biofilters measured here has
also been noted in other seaweed biofilters (DeBoer et al., 1978; Neori et al., 1996).
Macroalgae grown in artificially enriched media are typically supplied with inorganic nitrogen and phosphorous at molar ratios of 1013:1, N:P (Vandermeulen
and Gordin, 1990; Friedlander et al., 1991; Ugarte and Santelices, 1992; Israel et
al., 1995). In the present system, inorganic nutrients were added in accordance with
the higher Redfield ratio for phytoplankton cells, N:P= 16:1. Despite this elevated
ratio, phosphorous removal efficiency was low.
In the G. conferta biofilter, high nitrogen filtration efficiencies in spring 1995
could not be accounted for by a correspondingly high production of Gracilaria
tissue. It is considered likely that nitrogen was removed from the water by
autotrophic fouling organisms; apart from the visibly obvious presence of macroscopic chlorophytes, small quantities of oxidized nitrogen were frequently detected
in the effluents of this tank. It is therefore possible that there, the same nitrificationdenitrification coupled processes competed with the G. conferta for ammonia, as
found by Dvir (1995), and created large N-deficits. Gracilaria conferta has always

236

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

been an inferior grower in Eilat, and therefore it is not dependable as a biofilter.

However, with special care it can be cultured, as a supplement to the U. lactuca
culture.
In both biofilters a large proportion of the nitrogen supplied was removed as
surplus seaweed production and only a very small fraction as abalone biomass
(2.2%), implying that the ratio of abalone biomass to algal production unit size,
and hence the abalone production, was far too low. The results of the present study
make it possible to determine a more appropriate ratio and estimate the subsequent
system productivity.
Owing to the unreliable performance of the G. conferta biofilter, the following
calculations are based on integrated abalone/Ul6a tanks, stocked with animals of
the size range used here, typical of second-year growout H. tuberculata (Mgaya and
Mercer, 1994). Assuming a steady annual ingestion rate of 5.9% body weight d 1,
and mean U. lactuca production of 230 g m 2 d 1 (49% N-filtration efficiency,
58% if N-recycling is excluded), and using the more conservative parameters of the
abalone population from tank A (mean FCR=20; 45% of N entering the abalone
tank is released in tank effluents), an appropriately proportioned system can be
proposed. The productivity of such a system, standardized to 1 kg N input, is
compared to the original model of Shpigel and Neori (1996) in Table 7. The
performance of the experimental system studied here shows close agreement with
the predicted models.
This comparison provides also an indication of the benefits of the integration of
seaweed and abalone culture units into a single system. If the U. lactuca and
abalone were grown in separate systems, seawater supply would be doubled, the
nitrogen leaving the abalone vessel would be dumped into the sea and a corresponding amount of nitrogen (up to 24% in the 27 March 1996 experiment) would
have to be added to the U. lactuca culture. Hence, using this example, separating
the culture units would result in the need to supply an additional 24% nitrogen to
the algal unit and a similar (all the abalone effluents N) increase in nitrogen release
to the environment.
Although the production estimated possible by the data from the present study
(Table 7) compares closely with the projected yields suggested by Shpigel and Neori
(1996), it is unrealistic in the use of mean annual U. lactuca production to calculate
the corresponding biofilter size needed to provide food for the abalone. In reality,
if a single U. lactuca culture was used, the filter would have to provide sufficient
production during minimum winter growth (mean 82 g Ul6a m 2 d 1), this would
require a filter 2.8 times larger than proposed by the model. A more practical
solution would be to introduce a second U. lactuca biofilter in series, to serve as a
polishing filter, further reducing nutrient loading in system effluents, as successfully
applied by Lapointe et al. (1976), Krom et al. (1995) and Neori et al. (1996); the
second filter would also provide an additional source of U. lactuca biomass if the
production from the first filter fails to meet demands.
The level of inorganic nitrogen and N:P necessary to produce U. lactuca of
optimum nutritional value, while minimizing the level of nutrients in the effluent,
still needs to be determined and corrected for nitrogen supplied by abalone

A. Neori et al. / Aquacultural Engineering 17 (1998) 215239

237

effluents. The commercial application of such a system would also benefit from the
use of an improved abalone vessel design that does not permit excessive free
movement of animals and subsequent crowding problems, as recommended by
Fleming and Hone (1996), e.g. by use of suspended shelters or cages.
An additional recent finding can allow a significant reduction in the ratio of algae
biofilter area to kilogram of cultured abalone. Supplying ammonia-N influx at
double the rates used here has increased significantly the seaweed protein content
(see also in Cohen and Neori, 1991), a feature which has been shown by us to
reduce the FCR for the abalone by about half (Ragg et al., in preparation). As G.
conferta has been a useful dietary supplement it is suggested that the rhodophyte be
grown in a separate temperature regulated culture, receiving weekly nutrient pulses.
This can further reduce the area of seaweed biofilter per kilogram of reared
abalone.

Acknowledgements
The authors would like to offer special thanks to A. Marshall for valuable
observations as system manager; our gratitude also to D. Ben-Ezra, R. Fridman
and B. Simpson for their expert technical advice and assistance, to O. Dvir and I.
Lupatsch who performed the chemical analyses, and to A. Colorni and R. Goldberg for critical reviews of the manuscript. The project was supported by the Israeli
Ministry for Energy and Infrastructure and by a joint program of the EC and the
Israeli Ministry for Science (Grant No. 4564192 to M.S. and A.N.).

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