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A sustainable integrated system for culture of fish, seaweed and abalone
Aquaculture 186 Ž2000. 279–291 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 Ž Haliotis discus hannai . culture tanks drained into a pellet-fed fish Ž Sparus aurata. culture tank. The fish effluent drained into macroalgal ŽUlÕa 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 my2 yeary1. The nutrients excreted by the fish supported high yields of U. lactuca Ž78-kg my2 yeary1 . and efficient Ž80%. ammonia filtration. Gracilaria functioned poorly. UlÕa supported an abalone growth rate of 0.9% dayy1 and a length increase of 40–66 mm dayy1 in juveniles, and 0.34% dayy1 and 59 mm 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. q 2000 Elsevier Science B.V. All rights reserved. Keywords: Integrated; Land-based; Sustainable; Mariculture; Abalone; Fish; Seaweed; Nutrient-budget
E-mail address: [email protected] ŽA. Neori.. Corresponding author. Tel.: q9-727-636-1400, q9-727-636-1441, q9-727-636-1445; fax: q9-7276375761. )
0044-8486r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 Ž 9 9 . 0 0 3 7 8 - 6
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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 their ingested protein N, 80% of it in dissolved forms ŽPorter 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 for Mariculture ŽNCM., Eilat, for solving the effluent problem by nutrient recycling. Water from fishponds recirculates through biofilters of seaweed, which remove most of the ammonia from the water ŽCohen 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. Abalone is a commercially valuable marine gastropod ŽOakes and Ponte, 1996.. Its culture worldwide is severely limited by supplies of suitable seaweed ŽUki and Watanabe, 1992.. This situation makes it only natural to add abalone to the integrated culture system for fish and seaweed ŽShpigel and Neori, 1996.. The integrated culture of two organisms, abalone and seaweed, has been tested on a laboratory scale ŽNeori 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 The experimental system was a modification of our model design Ždesign 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, finfish, and seaweed. Unfiltered seawater Ž2400 l dayy1 . was pumped to two abalone tanks, drained through a fish tank, and finally through a seaweed filtrationrproduction unit back to the sea ŽFig. 1, gray rectangles.. The fish were fed with fish feed ŽMatmor, 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. 2.1. Abalone unit
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Fig. 1. A schematic diagram of the integrated mariculture system Žgray rectangles.. The processes defining the nitrogen budget are illustrated. Rounded values Žgrams N yeary1 . 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 were elevated, allowing effluents to drain into the fish tank. A removable screen Ž1-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 separate tanks, 1200 juveniles of 11 " 2.3 mm Žmean " sd. length Ž0.23 " 0.04 g. in one tank ŽGroup I. and 251 adults of 44.2 " 2 mm length Ž15.7 " 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 ŽGroup III.. 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 rates ŽSGR%. for each time interval, i.e., the percent body weight gain per day ŽShpigel et al., 1996, based on Day and Fleming, 1992. SGR%s Ž w lnWtylnW0 x rt . = 100 Ž 1.
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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. Shell length measurements were used to calculate shell growth Shell growth Ž m mrdayy1 . s Ž L2yL1 . rt
Ž 2.
where t is time interval in days, L1 is the length of an animal at the beginning of each monitoring interval and L2 is the length at the end of the interval. Food conversion ratio ŽFCR. was calculated from feed intake and growth FCR s feed intake Ž g fw . rweight gain Ž g fw .
Ž 3.
Additionally, the cumulative yields of the three abalone groups and the supplied seaweed were used to calculate overall production FCR. 2.2. Fish unit Three hundred gilthead sea bream Ž Sparus aurata. with an average weight of 40 g Ž12 kg total weight. were stocked in a 600-l Ž1 m2 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 600-l Ž1 m2 surface area. tanks as described in Vandermeulen Ž1989.. 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 Abiotic parameters Žoxygen, temperature, pH. and ammonia levels were monitored twice a day Žat 0800 and 1400 h. in all components of the system. Ammonia levels were monitored by an electrode ŽIngold NH 3 Electrode Type 15-230-3000.. In addition, 24-h intensive measurements were carried out several times a year. During the intensive measurement periods, ammonia-N was measured by an autoanalizer ŽTechnicon AA-II. as in Neori et al. Ž1996.. Nitrogen content of the abalone and the seaweed tissue were measured by a CHN analyzer ŽPerkin Elmer.. Nitrogen levels of the abalone mucus, and fish and abalone feces were measured in preliminary experiments and were estimated for this experiment according to the actual sizes of the abalone.
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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 was lower in juveniles of the larger size than in small juveniles and in adults ŽTable 1; Fig. 2.. From October 1995 to December 1996 the juvenile abalone ŽGroup I. more then tripled their length and multiplied their weight by nearly 30 fold ŽTable 1.. They increased their weight on averaged by nearly 1% dayy1 and their length by 66.5 mm dayy1 . Their FCR was above 5 and the survival 75%. The adult abalone ŽGroup II. increased 25% in length and doubled their weight in half a year ŽTable 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 was better, at 95%. The juveniles in the second period ŽGroup 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 on average by only 40 mm dayy1 ŽTable 1.. Their FCR was intermediate between those of the other two groups ŽTable 1.. The total abalone yield was 9.4 kg yeary1 , with 40% meat and meat dw protein content of 75 " 1% Žmean " sd, n s 4.. 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 mg ly1 . Annual fish production was 28 kg Ž35 kg my3 .. The fish grew in a year from 40 g to commercial weight of 470 g, but growth was slow in the summer months ŽFig. 3.. Average growth was 0.67% dayy1 , FCR averaged 2 and the survival was 95% ŽTable 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. The daily levels of pH Ž8.5–8.9. and dissolved oxygen Ž8.9–9.07 mg ly1 . were high, as typical for intensive photosynthetic culture. U. lactuca grew at a stable rate throughout the year, yielding on average 233 g fresh weight a day and 78 kg annually ŽFig. 4.. dw protein in this seaweed averaged 28 " 4% Ž n s 4.. 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 fragments ŽFig. 4., because of frequent culture crashes. dw protein content of this seaweed averaged 33 " 3% Ž n s 4.. The useful yield was given to the abalone, with the additional import of over 5 kg from another system.
284
Abalone I Ž374 days. Abalone II Ž184 days. Abalone III Ž224 days. Fish Ž374 days. a b
Initial weight Žg.
Final weight Žg.
Initial length Žmm.
Final length Žmm.
SGR% Ž% dayy1 .
Growth Žmm dayy1 .
FCR Žfwrfw.
Survival Ž%.
0.23"0.04 15.7"4.6 0.7"0.11 40.4"5.1
6.7"1.1 32.3"4.7 5.5"0.3 470"25
11.3"2.3 44.2"2.1 16.6"3.1 NA
36.2"4.4 55.1"5.2 33.7"3.7 NA
0.93 0.34 0.92 0.67
66.5 59 40 NA
5.16 14.2 8.26 2b
75 95 85 95
See detailed comparisons with published data in Shpigel et al. Ž1993. and in Table 2 of Shpigel et al. Ž1996.. dw feed per fw yield.
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Table 1 Growth parameters Žmean"sd. measured for the abalone and the fish in the integrated mariculture systema
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285
Fig. 2. Abalone average sizes Ž"sd. during the experiment. Abalone Group I Žl.; Abalone Group II Ž'.; Abalone Group III ŽX..
3.4. Ammonia monitoring The two daily values of ammonia electrode readings in each compartment were averaged daily and then monthly ŽFig. 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.
Fig. 3. Average weight per fish Žv . and growth rate Ž'. Ž"sd. of the fish during the experiment.
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Fig. 4. Seaweed cumulative yields during the experiment. U. lactuca Žl. and G. conferta Žv ..
3.5. Nitrogen transformations and budgets The analytical Žautoanalyser. 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. Inflow from the sea Žl.; abalone effluents ŽB.; fish effluents Ž"sd. Ž'.; Gracilaria effluents Žv .; UlÕa effluents ŽX..
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each of the three culture compartments and the fourth for the entire integrated culture system ŽTable 2.. 3.5.1. Abalone unit N-budget The only significant N input to this unit was seaweed protein. The abalone assimilated nearly 40% of this input N ŽTable 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 as dissolved N from the abalone tanks ŽTable 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 Unit
N-form
kg yeary1
g N yeary1
%
Abalone
Seaweed input Abalone harvest Effluent ammonia Feces and mucus Deficit
47 9.4
410 154 150"49 107 y1
100 38 37 26 0
Fish
Feed input Influent ammonia Fish harvest Effluent ammonia Feces Deficit
54
3918 150 768 1879"189 392 1030
Seaweed: UlÕa
Seaweed: Gracilaria
Whole System
Influent ammonia Harvest Effluent Ammonia Deficit Influent ammonia Harvest Fragments Effluent ammonia Deficit Feed input Fish yield Fish feces UlÕa yield UlÕa exported Gracilaria yield Gracilaria discarded Gracilaria imported Abalone yield Abalone feces and mucus Ammonia in effluents Deficit
28
78
7 7
54 28 78 42 14 7 5.6 9.4
96 4 19 46 10 25
939 629 195"14 116
100 67 21 12
939 67 67 199"41 607
100 7 7 21 65
3918 768 392 629 339 134 67 53 154 107 393"54 1805
100 19 10 16 8.6 3.4 1.7 1.4 3.9 2.7 10 46
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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 forms of combined nitrogen Žnitrite, nitrate and DON, see Krom et al., 1995., algal growth on the walls and loss to denitrification ŽDvir et al., 1999.. 3.5.3. Seaweed units N-budgets Both seaweed tanks received equal amounts of nutrients. The UlÕa tank harvest removed on average 67% of its ammonia input ŽTable 2.. The Gracilaria tank performed inadequately, because of frequent frond disintegration Žas 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 The overall N-budget of the system ŽTable 2; Fig. 1. has fish feed as its major input. The outputs are of three categories: harvests Žfish, abalone, exported seaweed., ammonia in the seaweed effluents and a deficit Žconsisting 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. The harvest category, ) 38% of the N input, consisted of fish Ž19%., seaweed Ž) 19%, over half of it in exported and discarded biomass N. and abalone Ž4%.. 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 sustainability 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 pollution can be further reduced below 30% of input Žcompared 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 previous study ŽShpigel et al, 1996., we found that H. discus hannai grew about 15 mm
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Table 3 Data synopsisa : culture dimensions, stocking densities and annual yields of abalone, fish and seaweed. ŽA. Data from this experimental system; ŽB. System potential after adjustments in the abalone and seaweed units Dimensions culture Žm2 .
Density stocking Žkg my2 .
Yield annual Žkg.
(A) Data Abalone Fish Seaweed
0.3 1 2
13 b ; 25c 15 1–2 d ; 5–12 e
9.4 28 78 d ; 14 e
(B) Potential Abalone Fish Seaweed
0.6 1 2
13 b ; 25c 15 1–2 d
19 28 156
a
See detailed comparisons with published data in Shpigel et al. Ž1993. and in Table 2 of Shpigel et al. Ž1996.. b Juvenile abalone. c Adult abalone. d UlÕa lactuca. e Gracilaria conferta.
in the first year Ž37 mm dayy1 ., with an FCR of 20. In the integrated system described here, the growth in the first year has improved to nearly 22 mm Ž66 mm dayy1 .. This value is similar to the 64 mm dayy1 reported from Northern China ŽNie, 1992., but still falls short of the reported values of 80–100 mm dayy1 in Korea ŽYoo, 1989. and 80–120 mm dayy1 in Japan ŽHahn, 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 body weight, compared with about 10% noted by Yoo Ž1989.. 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 seabream Žcf. Shpigel et al., 1993., suggesting the system provided the fish with adequate growth conditions. As we have found earlier ŽPorter 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 N content, agree with our earlier results ŽNeori et al., 1996, 1998; Shpigel et al., 1999.. Gracilaria performance was poor, as in Neori et al. Ž1998.. Until further advances are made, this seaweed is not fit for use in the type of mariculture biofilters described here. According to Shpigel and Neori Ž1996., the yield Žkg 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 study ŽTable 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 have been 1000:6000:680 ŽTable 3B.. In other words, the production of 1 t of fish potentially supports the additional production of 2r3 t of abalone.
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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 m 2 devoted to abalone:fish:seaweed, respectively ŽTable 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. Of the remaining 73% of the N-budget, much will be reduced N Žammonia 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 dayy1 Ž13 kg feed. in fish feed protein will daily produce in this system over 7 kg fish ŽUS$50. and 4.8 kg abalone ŽUS$230.. It will do so using 330 m2 of mariculture ponds Ž90 m2 of a fishpond, 180 m2 of a seaweed pond and 60 m2 of abalone tanks.. In a 120-m2 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 Infrastructure, by Seaor Marine and by a joint program of the EC and the Israeli Ministry for Science ŽGrant No. 4564192 to M.S. and A.N...
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Dvir, O., Van Rijn, J., Neori, A., 1999. Nitrogen transformations and factors leading to nitrite accumulation in a hypertrophic marine fish culture system. Mar. Ecol. Prog. Ser. 181, 97–106. Hahn, K.O., 1989. Japanese abalone culture techniques of the Oyster Research Institute. In: Hahn, K.O. ŽEd.., CRC Handbook of Culture of Abalone and Other Marine Gastropods. CRC Press, Boca Raton, FL, pp. 195–220. Krom, M.D., Ellner, J., van Rijn, J., Neori, A., 1995. Nitrogen and phosphorous cycling and transformations in a prototype ‘non-polluting’ integrated mariculture system, Eilat, Israel. Mar. Ecol. Prog. Ser. 118, 25–36. Krom, M.D., Neori, A., 1989. A total nutrient budget for an experimental fishpond with circularly moving seawater. Aquaculture 83, 345–358. Neori, A., Ellner, S.P., Boyd, C.E., Krom, M.D., 1993. The integration of seaweed biofilters with intensive fish ponds to improve water quality and recapture nutrients. In: Moshiri, G.A. ŽEd.., Constructed Wetlands for Water Quality Improvement. Lewis Publishers, Boca Raton, FL, pp. 603–607. Neori, A., Krom, M.D., Ellner, S.P., Boyd, C.E., Popper, D., Rabinovitch, R., Davison, P.J., Dvir, O., Zuber, D., Ucko, M., Angel, D., Gordin, H., 1996. Seaweed biofilters as regulators of water quality in integrated fish–seaweed culture units. Aquaculture 141, 183–199. Neori, A., Ragg, N.L.C., Shpigel, M., 1998. The integrated culture of seaweed, abalone, fish and clams in modular intensive land-based systems: II. Performance and nitrogen partitioning within an abalone Ž Haliotis tuberculata. and macroalgae culture system. Aquacult. Eng. 17, 215–239. Nie, Z.Q., 1992. A review of abalone culture in China. In: Shepherd, S.A., Tegner, M.J., Guzman del Proo, S.A. ŽEds.., Abalone of the World: Biology, Fisheries and Culture. Blackwell, Oxford, pp. 592–602. Oakes, F.R., Ponte, R.D., 1996. The abalone market: opportunities for cultured abalone. Aquaculture 140, 187–195. Porter, C.B., Krom, M.D., Robbins, M.G., Brickel, L., Davidson, A., 1987. Ammonia excretion and total N budget for Gilthead Seabream Ž Sparus aurata. and its effect of water quality conditions. Aquaculture 66, 287–297. Shpigel, M., Neori, A., 1996. The integrated culture of seaweed, abalone, fish and clams in modular intensive land-based systems: I. Proportions of size and projected revenues. Aquacult. Eng. 15, 313–326. Shpigel, M., Neori, A., Popper, D.M., Gordin, H., 1993. A proposed model for ‘‘environmentally clean’’ land-based culture of fish, bivalves and seaweeds. Aquaculture 117, 115–128. Shpigel, M., Neori, A., Marshall, A., 1996. The suitability of several introduced species of abalone Ž gastropoda: haliotidae . for land-based culture with pond growth seaweed in Israel. Isr. J. Aquacult. Bamidgeh 48, 192–200. Shpigel, M., Ragg, N.L., Lupatsch, I., Neori, A., 1999. Protein content determines the nutritional value of the seaweed UlÕa lactuca L for the abalone Haliotis tuberculata L. and H. Discus hannai Ino. J. Shellfish Res. 18, 1–7. Uki, N., Watanabe, T., 1992. Review of the nutritional requirements of abalone Ž Haliotis spp.. and development of more efficient artificial diets. In: Shepherd, S.A., Tegner, M.J., del Proo, S.A.G. ŽEds.., Abalone of the World: Biology, Fisheries and Culture. Fishing News Books, pp. 504–517. Vandermeulen, H., 1989. A low-maintenance tank for mass culture of seaweeds. Aquacult. Eng. 8, 67–71. Yoo, S.K., 1989. Abalone farming in Korea. In: Hahn, K.O. ŽEd.., CRC Handbook of Culture of Abalone and Other Marine Gastropods. CRC Press, Boca Raton, FL, pp. 255–263.
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 Ž Haliotis discus hannai . culture tanks drained into a pellet-fed fish Ž Sparus aurata. culture tank. The fish effluent drained into macroalgal ŽUlÕa 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 my2 yeary1. The nutrients excreted by the fish supported high yields of U. lactuca Ž78-kg my2 yeary1 . and efficient Ž80%. ammonia filtration. Gracilaria functioned poorly. UlÕa supported an abalone growth rate of 0.9% dayy1 and a length increase of 40–66 mm dayy1 in juveniles, and 0.34% dayy1 and 59 mm 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. q 2000 Elsevier Science B.V. All rights reserved. Keywords: Integrated; Land-based; Sustainable; Mariculture; Abalone; Fish; Seaweed; Nutrient-budget
E-mail address: [email protected] ŽA. Neori.. Corresponding author. Tel.: q9-727-636-1400, q9-727-636-1441, q9-727-636-1445; fax: q9-7276375761. )
0044-8486r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 Ž 9 9 . 0 0 3 7 8 - 6
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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 their ingested protein N, 80% of it in dissolved forms ŽPorter 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 for Mariculture ŽNCM., Eilat, for solving the effluent problem by nutrient recycling. Water from fishponds recirculates through biofilters of seaweed, which remove most of the ammonia from the water ŽCohen 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. Abalone is a commercially valuable marine gastropod ŽOakes and Ponte, 1996.. Its culture worldwide is severely limited by supplies of suitable seaweed ŽUki and Watanabe, 1992.. This situation makes it only natural to add abalone to the integrated culture system for fish and seaweed ŽShpigel and Neori, 1996.. The integrated culture of two organisms, abalone and seaweed, has been tested on a laboratory scale ŽNeori 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 The experimental system was a modification of our model design Ždesign 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, finfish, and seaweed. Unfiltered seawater Ž2400 l dayy1 . was pumped to two abalone tanks, drained through a fish tank, and finally through a seaweed filtrationrproduction unit back to the sea ŽFig. 1, gray rectangles.. The fish were fed with fish feed ŽMatmor, 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. 2.1. Abalone unit
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Fig. 1. A schematic diagram of the integrated mariculture system Žgray rectangles.. The processes defining the nitrogen budget are illustrated. Rounded values Žgrams N yeary1 . 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 were elevated, allowing effluents to drain into the fish tank. A removable screen Ž1-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 separate tanks, 1200 juveniles of 11 " 2.3 mm Žmean " sd. length Ž0.23 " 0.04 g. in one tank ŽGroup I. and 251 adults of 44.2 " 2 mm length Ž15.7 " 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 ŽGroup III.. 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 rates ŽSGR%. for each time interval, i.e., the percent body weight gain per day ŽShpigel et al., 1996, based on Day and Fleming, 1992. SGR%s Ž w lnWtylnW0 x rt . = 100 Ž 1.
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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. Shell length measurements were used to calculate shell growth Shell growth Ž m mrdayy1 . s Ž L2yL1 . rt
Ž 2.
where t is time interval in days, L1 is the length of an animal at the beginning of each monitoring interval and L2 is the length at the end of the interval. Food conversion ratio ŽFCR. was calculated from feed intake and growth FCR s feed intake Ž g fw . rweight gain Ž g fw .
Ž 3.
Additionally, the cumulative yields of the three abalone groups and the supplied seaweed were used to calculate overall production FCR. 2.2. Fish unit Three hundred gilthead sea bream Ž Sparus aurata. with an average weight of 40 g Ž12 kg total weight. were stocked in a 600-l Ž1 m2 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 600-l Ž1 m2 surface area. tanks as described in Vandermeulen Ž1989.. 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 Abiotic parameters Žoxygen, temperature, pH. and ammonia levels were monitored twice a day Žat 0800 and 1400 h. in all components of the system. Ammonia levels were monitored by an electrode ŽIngold NH 3 Electrode Type 15-230-3000.. In addition, 24-h intensive measurements were carried out several times a year. During the intensive measurement periods, ammonia-N was measured by an autoanalizer ŽTechnicon AA-II. as in Neori et al. Ž1996.. Nitrogen content of the abalone and the seaweed tissue were measured by a CHN analyzer ŽPerkin Elmer.. Nitrogen levels of the abalone mucus, and fish and abalone feces were measured in preliminary experiments and were estimated for this experiment according to the actual sizes of the abalone.
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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 was lower in juveniles of the larger size than in small juveniles and in adults ŽTable 1; Fig. 2.. From October 1995 to December 1996 the juvenile abalone ŽGroup I. more then tripled their length and multiplied their weight by nearly 30 fold ŽTable 1.. They increased their weight on averaged by nearly 1% dayy1 and their length by 66.5 mm dayy1 . Their FCR was above 5 and the survival 75%. The adult abalone ŽGroup II. increased 25% in length and doubled their weight in half a year ŽTable 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 was better, at 95%. The juveniles in the second period ŽGroup 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 on average by only 40 mm dayy1 ŽTable 1.. Their FCR was intermediate between those of the other two groups ŽTable 1.. The total abalone yield was 9.4 kg yeary1 , with 40% meat and meat dw protein content of 75 " 1% Žmean " sd, n s 4.. 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 mg ly1 . Annual fish production was 28 kg Ž35 kg my3 .. The fish grew in a year from 40 g to commercial weight of 470 g, but growth was slow in the summer months ŽFig. 3.. Average growth was 0.67% dayy1 , FCR averaged 2 and the survival was 95% ŽTable 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. The daily levels of pH Ž8.5–8.9. and dissolved oxygen Ž8.9–9.07 mg ly1 . were high, as typical for intensive photosynthetic culture. U. lactuca grew at a stable rate throughout the year, yielding on average 233 g fresh weight a day and 78 kg annually ŽFig. 4.. dw protein in this seaweed averaged 28 " 4% Ž n s 4.. 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 fragments ŽFig. 4., because of frequent culture crashes. dw protein content of this seaweed averaged 33 " 3% Ž n s 4.. The useful yield was given to the abalone, with the additional import of over 5 kg from another system.
284
Abalone I Ž374 days. Abalone II Ž184 days. Abalone III Ž224 days. Fish Ž374 days. a b
Initial weight Žg.
Final weight Žg.
Initial length Žmm.
Final length Žmm.
SGR% Ž% dayy1 .
Growth Žmm dayy1 .
FCR Žfwrfw.
Survival Ž%.
0.23"0.04 15.7"4.6 0.7"0.11 40.4"5.1
6.7"1.1 32.3"4.7 5.5"0.3 470"25
11.3"2.3 44.2"2.1 16.6"3.1 NA
36.2"4.4 55.1"5.2 33.7"3.7 NA
0.93 0.34 0.92 0.67
66.5 59 40 NA
5.16 14.2 8.26 2b
75 95 85 95
See detailed comparisons with published data in Shpigel et al. Ž1993. and in Table 2 of Shpigel et al. Ž1996.. dw feed per fw yield.
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Table 1 Growth parameters Žmean"sd. measured for the abalone and the fish in the integrated mariculture systema
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285
Fig. 2. Abalone average sizes Ž"sd. during the experiment. Abalone Group I Žl.; Abalone Group II Ž'.; Abalone Group III ŽX..
3.4. Ammonia monitoring The two daily values of ammonia electrode readings in each compartment were averaged daily and then monthly ŽFig. 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.
Fig. 3. Average weight per fish Žv . and growth rate Ž'. Ž"sd. of the fish during the experiment.
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Fig. 4. Seaweed cumulative yields during the experiment. U. lactuca Žl. and G. conferta Žv ..
3.5. Nitrogen transformations and budgets The analytical Žautoanalyser. 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. Inflow from the sea Žl.; abalone effluents ŽB.; fish effluents Ž"sd. Ž'.; Gracilaria effluents Žv .; UlÕa effluents ŽX..
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each of the three culture compartments and the fourth for the entire integrated culture system ŽTable 2.. 3.5.1. Abalone unit N-budget The only significant N input to this unit was seaweed protein. The abalone assimilated nearly 40% of this input N ŽTable 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 as dissolved N from the abalone tanks ŽTable 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 Unit
N-form
kg yeary1
g N yeary1
%
Abalone
Seaweed input Abalone harvest Effluent ammonia Feces and mucus Deficit
47 9.4
410 154 150"49 107 y1
100 38 37 26 0
Fish
Feed input Influent ammonia Fish harvest Effluent ammonia Feces Deficit
54
3918 150 768 1879"189 392 1030
Seaweed: UlÕa
Seaweed: Gracilaria
Whole System
Influent ammonia Harvest Effluent Ammonia Deficit Influent ammonia Harvest Fragments Effluent ammonia Deficit Feed input Fish yield Fish feces UlÕa yield UlÕa exported Gracilaria yield Gracilaria discarded Gracilaria imported Abalone yield Abalone feces and mucus Ammonia in effluents Deficit
28
78
7 7
54 28 78 42 14 7 5.6 9.4
96 4 19 46 10 25
939 629 195"14 116
100 67 21 12
939 67 67 199"41 607
100 7 7 21 65
3918 768 392 629 339 134 67 53 154 107 393"54 1805
100 19 10 16 8.6 3.4 1.7 1.4 3.9 2.7 10 46
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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 forms of combined nitrogen Žnitrite, nitrate and DON, see Krom et al., 1995., algal growth on the walls and loss to denitrification ŽDvir et al., 1999.. 3.5.3. Seaweed units N-budgets Both seaweed tanks received equal amounts of nutrients. The UlÕa tank harvest removed on average 67% of its ammonia input ŽTable 2.. The Gracilaria tank performed inadequately, because of frequent frond disintegration Žas 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 The overall N-budget of the system ŽTable 2; Fig. 1. has fish feed as its major input. The outputs are of three categories: harvests Žfish, abalone, exported seaweed., ammonia in the seaweed effluents and a deficit Žconsisting 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. The harvest category, ) 38% of the N input, consisted of fish Ž19%., seaweed Ž) 19%, over half of it in exported and discarded biomass N. and abalone Ž4%.. 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 sustainability 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 pollution can be further reduced below 30% of input Žcompared 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 previous study ŽShpigel et al, 1996., we found that H. discus hannai grew about 15 mm
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Table 3 Data synopsisa : culture dimensions, stocking densities and annual yields of abalone, fish and seaweed. ŽA. Data from this experimental system; ŽB. System potential after adjustments in the abalone and seaweed units Dimensions culture Žm2 .
Density stocking Žkg my2 .
Yield annual Žkg.
(A) Data Abalone Fish Seaweed
0.3 1 2
13 b ; 25c 15 1–2 d ; 5–12 e
9.4 28 78 d ; 14 e
(B) Potential Abalone Fish Seaweed
0.6 1 2
13 b ; 25c 15 1–2 d
19 28 156
a
See detailed comparisons with published data in Shpigel et al. Ž1993. and in Table 2 of Shpigel et al. Ž1996.. b Juvenile abalone. c Adult abalone. d UlÕa lactuca. e Gracilaria conferta.
in the first year Ž37 mm dayy1 ., with an FCR of 20. In the integrated system described here, the growth in the first year has improved to nearly 22 mm Ž66 mm dayy1 .. This value is similar to the 64 mm dayy1 reported from Northern China ŽNie, 1992., but still falls short of the reported values of 80–100 mm dayy1 in Korea ŽYoo, 1989. and 80–120 mm dayy1 in Japan ŽHahn, 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 body weight, compared with about 10% noted by Yoo Ž1989.. 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 seabream Žcf. Shpigel et al., 1993., suggesting the system provided the fish with adequate growth conditions. As we have found earlier ŽPorter 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 N content, agree with our earlier results ŽNeori et al., 1996, 1998; Shpigel et al., 1999.. Gracilaria performance was poor, as in Neori et al. Ž1998.. Until further advances are made, this seaweed is not fit for use in the type of mariculture biofilters described here. According to Shpigel and Neori Ž1996., the yield Žkg 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 study ŽTable 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 have been 1000:6000:680 ŽTable 3B.. In other words, the production of 1 t of fish potentially supports the additional production of 2r3 t of abalone.
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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 m 2 devoted to abalone:fish:seaweed, respectively ŽTable 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. Of the remaining 73% of the N-budget, much will be reduced N Žammonia 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 dayy1 Ž13 kg feed. in fish feed protein will daily produce in this system over 7 kg fish ŽUS$50. and 4.8 kg abalone ŽUS$230.. It will do so using 330 m2 of mariculture ponds Ž90 m2 of a fishpond, 180 m2 of a seaweed pond and 60 m2 of abalone tanks.. In a 120-m2 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 Infrastructure, by Seaor Marine and by a joint program of the EC and the Israeli Ministry for Science ŽGrant No. 4564192 to M.S. and A.N...
References Cohen, I., Neori, A., 1991. UlÕa lactuca biofilters for marine fishpond effluent: I. Ammonia uptake kinetics and nitrogen content. Bot. Mar. 34, 475–482. Day, R., Fleming, E., 1992. The determinants and measurement of abalone growth. In: Shepherd, S.A., Tegner, M.J., del Proo, S.A.G. ŽEds.., Abalone of the World: Biology, Fisheries and Culture. Fishing News Books, pp. 141–168.
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