www.elsevier.nlrlocateraqua-online
A sustainable integrated system for culture of fish,
seaweed and abalone
Amir Neori
), Muki Shpigel, David Ben-Ezra
Israel Oceanographic and Limnological Research, National Center for Mariculture, P.O. Box 1212, Elat, 88112, Israel
Accepted 2 December 1999
Abstract
A 3.3 m2 experimental system for the intensive land-based culture of abalone, seaweed and
fish was established using an integrated design. The goals were to achieve nutrient recycling, reduced water use, reduced nutrient discharge and high yields. Effluents from Japanese abalone
ŽHaliotis discus hannai culture tanks drained into a pellet-fed fish Sparus aurata culture tank.. Ž .
Ž .
The fish effluent drained into macroalgal UlÕa lactuca or Gracilaria conferta culture, and
biofilter tanks. Algal production fed the abalone. The system was monitored to assess productivity and nitrogen partitioning over a year. The fish grew at 0.67% dayy1, yielding 28-kg my2yeary1.
Ž y2 y1.
The nutrients excreted by the fish supported high yields of U. lactuca 78-kg m year and
Ž .
efficient 80% ammonia filtration. Gracilaria functioned poorly. UlÕa supported an abalone
growth rate of 0.9% dayy1and a length increase of 40–66mm dayy1 in juveniles, and 0.34%
dayy1and 59mm dayy1
in young adults. Total abalone yield was 9.4 kg yeary1. A surplus of seaweed was created in the system. Ammonia-N, as a fraction of total feed-N was reduced from 45% in the fish effluents to 10% in the post-seaweed discharge. Based on the results, a doubling of the abalone:fish yield ratio from 0.3 to 0.6 is feasible.q2000 Elsevier Science B.V. All rights reserved.
Keywords: Integrated; Land-based; Sustainable; Mariculture; Abalone; Fish; Seaweed; Nutrient-budget
Ž .
E-mail address: neori@ocean.org.il A. Neori .
)Corresponding author. Tel.: q9-727-636-1400, q9-727-636-1441, q9-727-636-1445; fax: q
9-727-6375761.
0044-8486r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved.
Ž .
( ) A. Neori et al.rAquaculture 186 2000 279–291 280
1. Introduction
The discharge of low-quality water from intensive land-based mariculture facilities causes environmental and economic concerns, since fish excrete to the water 70–80% of
Ž .
their ingested protein N, 80% of it in dissolved forms Porter et al., 1987 . The development of practical and non-polluting land-based maricultural practices is therefore of great importance, both for mariculture and for the coastal environment.
A useful approach of integrated mariculture has been designed at the National Center Ž .
for Mariculture NCM , Eilat, for solving the effluent problem by nutrient recycling. Water from fishponds recirculates through biofilters of seaweed, which remove most of
Ž .
the ammonia from the water Cohen and Neori, 1991; Neori et al., 1993, 1996 . The financial return from the low-value seaweed biomass by-product can be raised greatly by feeding it to valuable macroalgivores, such as sea urchins and abalone.
Ž .
Abalone is a commercially valuable marine gastropod Oakes and Ponte, 1996 . Its Ž
culture worldwide is severely limited by supplies of suitable seaweed Uki and Watan-.
abe, 1992 . This situation makes it only natural to add abalone to the integrated culture
Ž .
system for fish and seaweed Shpigel and Neori, 1996 . The integrated culture of two Ž
organisms, abalone and seaweed, has been tested on a laboratory scale Neori et al., .
1998 .
In this study, we describe the performance of a more complex system, for integrated culture of three organisms — abalone, fish and seaweed. The system is intended to be fully integrated, that is, the fluxes of water and nutrients between the three modules are adjusted to optimize water use, nutrient recycling and marketable production. The system is also intended to be sustainable, one that allows increased supply of marketable marine organisms with minimal increases in pollution and in burden on natural populations.
2. Materials and methods
Ž
The experimental system was a modification of our model design design B in .
Shpigel and Neori, 1996 , with a water saving modification, by which the abalone culture water were recycled for the fish culture. It consisted of one unit each for abalone,
Ž y1.
finfish, and seaweed. Unfiltered seawater 2400 l day was pumped to two abalone tanks, drained through a fish tank, and finally through a seaweed filtrationrproduction
Ž . Ž
unit back to the sea Fig. 1, gray rectangles . The fish were fed with fish feed Matmor, .
Israel . Ammonia and other nutrients excreted by the fish were removed by the seaweed and supported their growth. The seaweed was harvested and fed to the abalone. The integrated culture was operated for a year, beginning in October 1995.
Ž .
Fig. 1. A schematic diagram of the integrated mariculture system gray rectangles . The processes defining the
Ž y1.
nitrogen budget are illustrated. Rounded values grams N year quantify each process; solid vertical arrows are seawater flows; heavy dashed arrows are N inputs and outputs; the fine dashed line is seaweed recycling to the abalone.
The abalone unit consisted of two 120-l rectangular bottom drained tanks. The tanks Ž were elevated, allowing effluents to drain into the fish tank. A removable screen 1-cm
.
mesh covered the whole area 10 cm above the flat bottom, and retained the abalone while allowing feces and detritus to drain. The tanks were completely flushed and cleaned once a week. Two parallel air diffusers suspended the algae, which were added as feed. Two 160-mm diameter half pipes were stacked on the netting to provide surface area and shelter for abalone attachment.
Two size groups of Japanese abalone, Haliotis discus hannai, were stocked in
Ž . Ž .
separate tanks, 1200 juveniles of 11"2.3 mm mean"sd length 0.23"0.04 g in
Ž . Ž .
one tank Group I and 251 adults of 44.2"2 mm length 15.7"4.6 g in a second tank ŽGroup II . The juveniles were kept in the system 374 days. Six hundred juveniles were. culled out after 184 days. The adults were kept in the system at stocking densities of 20–30 kg my3. After 184 days they were harvested, measured for the parameters described below, and then replaced by 600 smaller individuals of 16.6"3.1 mm length Ž0.7"0.1 g for an additional 224 days Group III .. Ž .
One hundred animals in each adult group were individually tagged. Once a month the tagged animals were washed free of debris, drained to remove surplus water and dried on absorbent paper. Wet weight measurements were used to calculate specific growth
Ž . Ž
rates SGR% for each time interval, i.e., the percent body weight gain per day Shpigel .
et al., 1996, based on Day and Fleming, 1992
w
x
( ) A. Neori et al.rAquaculture 186 2000 279–291 282
where W is the wet weight of an animal at the beginning of each monitoring interval0 and W is the weight after t days of growth, at the end of the interval. Shell lengtht
measurements were used to calculate shell growth
Shell growth
Ž
mmrdayy1.
sŽ
L2yL1.
rtŽ .
2where t is time interval in days, L is the length of an animal at the beginning of each1 monitoring interval and L is the length at the end of the interval. Food conversion ratio2 ŽFCR was calculated from feed intake and growth.
FCRsfeed intake g fw
Ž
.
rweight gain g fwŽ
.
Ž .
3Additionally, the cumulative yields of the three abalone groups and the supplied seaweed were used to calculate overall production FCR.
2.2. Fish unit
Ž .
Three hundred gilthead sea bream Sparus aurata with an average weight of 40 g Ž12 kg total weight were stocked in a 600-l 1 m. Ž 2 surface area rectangular aerated. tank. The fish were fed a 45% protein pellet diet. The bottom of the tank was drained daily to remove feces and uneaten food. Stocking density was maintained below 15 kg my3. Excess fish were culled regularly. Once a month a sample of 50 fish was weighed. Specific growth rates and FCR were calculated as mentioned above.
2.3. Seaweed unit
Two species of seaweed, UlÕa lactuca and Gracilaria conferta, were grown in two
Ž 2 . Ž .
600-l 1 m surface area tanks as described in Vandermeulen 1989 . The algae were suspended in the water column by air diffusers situated at the bottom. Total seaweed biomass was kept approximately at 1.5 kg of U. lactuca and 5–13 kg of G. conferta. Twice a week, excess seaweed biomass was harvested. The seaweed was drained of surplus water and weighed. The biomass was fed to the abalone as needed and the rest discarded. Several crashes of the G. conferta stock occurred, necessitating biomass imports.
2.4. Abiotic parameters and nitrogen budgets
Ž .
Abiotic parameters oxygen, temperature, pH and ammonia levels were monitored
Ž .
twice a day at 0800 and 1400 h in all components of the system. Ammonia levels were
Ž .
monitored by an electrode Ingold NH Electrode Type 15-230-3000 . In addition, 24-h3 intensive measurements were carried out several times a year. During the intensive
Ž .
measurement periods, ammonia-N was measured by an autoanalizer Technicon AA-II Ž .
as in Neori et al. 1996 . Nitrogen content of the abalone and the seaweed tissue were
Ž .
measured by a CHN analyzer Perkin Elmer .
3. Results
3.1. Abalone unit
Average water temperature in the abalone tanks ranged from 208C in winter to 288C in summer. Levels of pH, oxygen and salinity were stable throughout the year and ranged between 7.4–7.6, 7.8–8.8 mg l-1 and 40–41 ppt, respectively.
Growth rate by weight slowed as the animals grew larger, but growth rate by length Ž
was lower in juveniles of the larger size than in small juveniles and in adults Table 1;
. Ž .
Fig. 2 . From October 1995 to December 1996 the juvenile abalone Group I more then Ž . tripled their length and multiplied their weight by nearly 30 fold Table 1 . They increased their weight on averaged by nearly 1% dayy1 and their length by 66.5mm
y1 Ž .
day . Their FCR was above 5 and the survival 75%. The adult abalone Group II Ž .
increased 25% in length and doubled their weight in half a year Table 1 . Daily growth averaged only 0.34% by weight, but nearly equalled the juveniles’ length increase at 59 mm dayy1. FCR of the adults was nearly triple that of the juveniles, 14.2, but survival
Ž .
was better, at 95%. The juveniles in the second period Group III gained in weight nearly 8 fold and doubled their length in 224 days. Their daily growth averaged about the same as that of the juveniles from Group I, at nearly 1%, while their length increased
y1 Ž .
on average by only 40mm day Table 1 . Their FCR was intermediate between those
Ž . y1
of the other two groups Table 1 . The total abalone yield was 9.4 kg year , with 40%
Ž .
meat and meat dw protein content of 75"1% mean"sd, ns4 .
3.2. Fish unit
Average water temperature in the fish tank ranged from 19.18C in winter to 27.98C in summer. Salinity levels were constant throughout the year at 41 ppt. The pH levels ranged between 7.1–8.0. Oxygen levels were relatively low and ranged between 2.5–6.3
y1 Ž y3.
mg l . Annual fish production was 28 kg 35 kg m . The fish grew in a year from 40 Ž . g to commercial weight of 470 g, but growth was slow in the summer months Fig. 3 .
y1 Ž
Average growth was 0.67% day , FCR averaged 2 and the survival was 95% Table .
1 .
3.3. Seaweed unit
Water temperature in the seaweed tanks ranged from 18.18C in winter to average temperature of 31.28C in summer. Salinity was stable and at 41 ppt throughout the year.
Ž . Ž y1.
The daily levels of pH 8.5–8.9 and dissolved oxygen 8.9–9.07 mg l were high, as typical for intensive photosynthetic culture. U. lactuca grew at a stable rate throughout
Ž . the year, yielding on average 233 g fresh weight a day and 78 kg annually Fig. 4 . dw
Ž .
protein in this seaweed averaged 28"4% ns4 . Only 46% of the yield was transferred to the abalone, the rest was harvested.
Annual production of G. conferta was poor, only 14 kg, of which half was in useless Ž .
fragments Fig. 4 , because of frequent culture crashes. dw protein content of this Ž .
()
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Table 1
Ž . a
Growth parameters mean"sd measured for the abalone and the fish in the integrated mariculture system
Initial weight Final weight Initial length Final length SGR% Growth FCR Survival
y1 y1
Ž .g Ž .g Žmm. Žmm. Ž% day . Žmm day . Žfwrfw. Ž .%
Ž .
Abalone I 374 days 0.23"0.04 6.7"1.1 11.3"2.3 36.2"4.4 0.93 66.5 5.16 75
Ž .
Abalone II 184 days 15.7"4.6 32.3"4.7 44.2"2.1 55.1"5.2 0.34 59 14.2 95
Ž .
Abalone III 224 days 0.7"0.11 5.5"0.3 16.6"3.1 33.7"3.7 0.92 40 8.26 85 b
Ž .
Fish 374 days 40.4"5.1 470"25 NA NA 0.67 NA 2 95
a Ž . Ž .
See detailed comparisons with published data in Shpigel et al. 1993 and in Table 2 of Shpigel et al. 1996 . b
Ž . Ž . Ž .
Fig. 2. Abalone average sizes "sd during the experiment. Abalone Group I l; Abalone Group II ';
Ž .
Abalone Group III X .
3.4. Ammonia monitoring
The two daily values of ammonia electrode readings in each compartment were Ž .
averaged daily and then monthly Fig. 5 . Inflow ammonia concentration was negligible, and the abalone added only a little ammonia to the water. The fish compartment produced the bulk of the ammonia, which was then consistently removed by both seaweed tanks.
Ž . Ž . Ž .
( ) A. Neori et al.rAquaculture 186 2000 279–291 286
Ž . Ž .
Fig. 4. Seaweed cumulative yields during the experiment. U. lactuca l and G. conferta v.
3.5. Nitrogen transformations and budgets
Ž .
The analytical autoanalyser nitrogen data from three sampling dates, in April, July and November, have been averaged and condensed into four nitrogen budgets, one for
Fig. 5. Daily monitoring of ammonia concentrations in the water, averaged for each month, at the different compartments of the integrated mariculture system. Measurements were taken with an ammonia electrode.
Ž . Ž . Ž . Ž . Ž .
Inflow from the sea l; abalone effluents B; fish effluents "sd '; Gracilaria effluents v; UlÕa
Ž .
each of the three culture compartments and the fourth for the entire integrated culture Ž .
system Table 2 .
3.5.1. Abalone unit N-budget
The only significant N input to this unit was seaweed protein. The abalone assimi-Ž .
lated nearly 40% of this input N Table 2 . Over 60% of the input was unassimilated nitrogen, released from the abalone vessels as ammonia, feces and mucus.
3.5.2. Fish unit N-budget
The major N input to the fish tank was protein in the feed as well as a small quantity Ž .
as dissolved N from the abalone tanks Table 2 . The fish assimilated nearly 20% of this
Table 2
Nitrogen budgets of each unit of the integrated mariculture system and of the whole system
y1 y1
Unit N-form kg year g N year %
Abalone Seaweed input 47 410 100
Abalone harvest 9.4 154 38
Effluent ammonia 150"49 37
Feces and mucus 107 26
Deficit y1 0
Fish Feed input 54 3918 96
Influent ammonia 150 4
Fish harvest 28 768 19
Effluent ammonia 1879"189 46
Feces 392 10
Deficit 1030 25
Seaweed: UlÕa Influent ammonia 939 100
Harvest 78 629 67
Effluent Ammonia 195"14 21
Deficit 116 12
Seaweed: Gracilaria Influent ammonia 939 100
Harvest 7 67 7
Fragments 7 67 7
Effluent ammonia 199"41 21
Deficit 607 65
Whole System Feed input 54 3918 100
Fish yield 28 768 19
Abalone feces and mucus 107 2.7
Ammonia in effluents 393"54 10
( ) A. Neori et al.rAquaculture 186 2000 279–291 288
quantity. Fifty six% of the input was unassimilated nitrogen, released from the fish tank as ammonia and feces. A deficit of 25% was presumably comprised of unmeasured
Ž .
forms of combined nitrogen nitrite, nitrate and DON, see Krom et al., 1995 , algal
Ž .
growth on the walls and loss to denitrification Dvir et al., 1999 .
3.5.3. Seaweed units N-budgets
Both seaweed tanks received equal amounts of nutrients. The UlÕa tank harvest
Ž .
removed on average 67% of its ammonia input Table 2 . The Gracilaria tank Ž
performed inadequately, because of frequent frond disintegration as in Neori et al., .
1998 . This resulted in an N deficit that constituted about 16% of the input to the entire integrated system. The Gracilaria deficit presumably consisted of algal growth on the walls, seaweed fragments, nitrate and DON.
3.5.4. Budget of the entire integrated system
Ž .
The overall N-budget of the system Table 2; Fig. 1 has fish feed as its major input.
Ž .
The outputs are of three categories: harvests fish, abalone, exported seaweed , ammonia Ž
in the seaweed effluents and a deficit consisting of unmeasured entities of dissolved N, .
particulate N, algal growth on the walls and denitrification . About a third of the deficit was contributed by the frond fragmentation in the Gracilaria culture.
Ž .
The harvest category, )38% of the N input, consisted of fish 19% , seaweed Ž)19%, over half of it in exported and discarded biomass N and abalone 4% .. Ž .
Had both seaweed tanks cultured UlÕa, the exported seaweed would have increased
to 32% and the deficit would have dropped below 30%.
4. Discussion
An integrated culture system can be defined as one where the sizes of the different culture units and the fluxes of nutrients through them are proportionate to each other. That is, the nutrient release by each unit just about matches the requirements of the following one. This condition increases nutrient recycling and therefore the sustainabil-ity of the technology. In the novel system described here, ammonia excreted by the fish supported high rates of seaweed growth and ammonia filtration. The produced seaweed was of sufficiently high protein content to support good abalone growth. A surplus of seaweed was created because of improved abalone FCR. The nitrogen that ended as pollution was reduced, compared with normal fish cage culture. The results indicate that
Ž
pollution can be further reduced below 30% of input compared with 70–80% in cage .
fish culture , by using UlÕa as the only seaweed biofilter and by doubling the quantity of
the abalone cultured.
4.1. Yields, dimensions and expected performance
Table 3 provides a synopsis of the dimensions and performance of the model integrated system. The yields of the three organisms in the experimental integrated system were equal to or better than those obtained in monocultures at the NCM. In a
Ž .
Table 3
a Ž .
Data synopsis : culture dimensions, stocking densities and annual yields of abalone, fish and seaweed. A
Ž .
Data from this experimental system; B System potential after adjustments in the abalone and seaweed units
Dimensions Density Yield annual
2 y2
Ž . Ž . Ž .
culture m stocking kg m kg
( )A Data
See detailed comparisons with published data in Shpigel et al. 1993 and in Table 2 of Shpigel et al.
Ž1996 ..
in the first year 37mm day , with an FCR of 20. In the integrated system described Ž y1. here, the growth in the first year has improved to nearly 22 mm 66 mm day . This
y1 Ž .
value is similar to the 64mm day reported from Northern China Nie, 1992 , but still
y1 Ž .
falls short of the reported values of 80–100 mm day in Korea Yoo, 1989 and
y1 Ž .
80–120mm day in Japan Hahn, 1989 .
The FCR for the abalone here was greatly improved compared with our previous data and data from the literature. The abalone also daily consumed U. lactuca at 7% of their
Ž .
body weight, compared with about 10% noted by Yoo 1989 . The reductions in ingested food and FCR are the result of supplying the abalone high-protein UlÕa
ŽShpigel et al., 1999 ..
The fish growth rate was similar to that achieved normally in the culture of the
Ž .
seabream cf. Shpigel et al., 1993 , suggesting the system provided the fish with Ž
adequate growth conditions. As we have found earlier Porter et al., 1987; Krom and .
Neori, 1989; Krom et al., 1995 , the fish assimilated nearly 20% of the protein N in their diet.
The UlÕa annually-averaged yield of over 230 g my2 dayy1, and the seaweed’s high
Ž .
N content, agree with our earlier results Neori et al., 1996, 1998; Shpigel et al., 1999 . Ž .
Gracilaria performance was poor, as in Neori et al. 1998 . Until further advances are
made, this seaweed is not fit for use in the type of mariculture biofilters described here.
Ž . Ž .
According to Shpigel and Neori 1996 , the yield kg fw ratio of fish:seaweed:abalone was expected to be 1000:6000:250; that is, the production of 1 t of fish leads to the additional production of 6 t seaweed, which generates 1r4 t of abalone. In the present
Ž .
study Table 3A , the fish:seaweed:abalone ratio figures were 1000:3000:320. Had the seaweed unit been all UlÕa, fed to an appropriate quantity of abalone, this ratio could
Ž .
( ) A. Neori et al.rAquaculture 186 2000 279–291 290
The dimensions of the units of the present experimental culture system were at an upper surface ratio of about 0.3:1:2 m2 devoted to abalone:fish:seaweed, respectively ŽTable 3A . With the expected increases in seaweed production due to the use of an all.
UlÕa seaweed system, and the proportional doubling of the abalone facility, the
recommended dimension ratio changes to about 0.6:1:2 m2 devoted to
Ž .
abalone:fish:seaweed, respectively Table 3B .
4.2. Nitrogen remoÕal
The present integrated system converted 23% of the nitrogen budget into fish and abalone flesh and additional 10.3% into exported seaweed. With an all-UlÕa seaweed
unit and a proportional increase in abalone culture capacity, using the data in the present study, 27% of the budget can become flesh of fish and abalone, with no seaweed export.
Ž .
Of the remaining 73% of the N-budget, much will be reduced N ammonia and DON , which can be recycled back into seaweed biofilters and support the culture of more abalone or other macroalgivores, upon further development of our technology.
4.3. Conclusions
The pilot mariculture system described here proves the practicality of land-based sustainable mariculture on the coasts of warm seas. Each of the organisms functioned in the integrated system as expected from our earlier single organism cultures or better Žcompare with Shpigel and Neori, 1996 . With these data, an input of 1 kg N day. y1 Ž13
. Ž .
kg feed in fish feed protein will daily produce in this system over 7 kg fish US$50
Ž . 2 Ž 2
and 4.8 kg abalone US$230 . It will do so using 330 m of mariculture ponds 90 m of
2 2 . 2
a fishpond, 180 m of a seaweed pond and 60 m of abalone tanks . In a 120-m pilot system under study at present, the practical and economic details of such an operation are being investigated.
Acknowledgements
We thank Prof. J. Mercer for valuable discussions, O. Dvir, Z. Ezer and I. Lupatsch for chemical analyses, L. Shauli for help in figure preparation and other members of the departments of shellfish research and of algae and water quality research at the NCM for their help. This study was supported by the Israeli Ministry for Energy and Infrastruc-ture, by Seaor Marine and by a joint program of the EC and the Israeli Ministry for
Ž .
Science Grant No. 4564192 to M.S. and A.N. .
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