The integrated culture of seaweed, abalone, fish and.pdf

Aquacultural Engineering 17 (1998) 215239

The integrated culture of seaweed, abalone, fish andclams 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 usingan integrated design aimed at eliminating the dependence on external food sources, whilstreducing water requirements and nutrient discharge levels. The system was the first andsimplest trial in a series of progressive complexity of the concept of integrated culture ofseaweed, abalone, fish and clams in modular and intensive land-based facilities. Relative sizesof the modules, their stocking densities and the rate of nutrient supply were determinedbased on earlier results to be optimal. Effluents from two abalone (Haliotis tuberculata)culture tanks drained into macroalgae (Ul6a lactuca or Gracilaria conferta) culture andbiofilter 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 forthe abalone. Excess algal yield was used elsewhere. The system was monitored to assessproductivity and nitrogen partitioning over a year, while improvements were made based onthe accumulating results. Total annual N-budgets were combined with mean productionfigures 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% and0.25% body weight:d in the two culture tanks; reduced growth and increased food conversionratios (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 produc-tion 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: [email protected]

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 comparedto the two organisms grown in monoculture. 1998 Elsevier Science B.V. All rightsreserved.

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 Islandsand the French Brittany coast, and the subsequent depletion in natural stocksduring the second half of the twentieth century have resulted in increasingly strictfishery legislation and reduced landings (Mgaya and Mercer, 1994). The continueddemand for abalone can not be met by the fishery. Therefore the feasibility ofculturing abalone has received some attention within the regions that previouslysupported its main fisheries (Hayashi, 1982; Hahn, 1989; Mgaya, 1995). The highvalue of H. tuberculata led to its introduction as a mariculture species into Irelandin 1976 (Mgaya and Mercer, 1994), and in 1993 at land-based facilities of the IsraeliNational Center for Mariculture (NCM), on the Gulf of Aqaba, Red Sea (Shpigeland Neori, 1996; Shpigel et al., 1996).

The development of commercial abalone culture is frequently limited by the needto acquire sufficient quantities of suitable dietary seaweed. Natural populations ofbrown or red algae are usually required, which are often in short supply (Mercer etal., 1993). However, large quantities of the ubiquitous chlorophyte Ul6a lactuca L.can be produced in seaweed culture systems, which serve as biofilters and areassociated with intensive seawater fishponds (Neori et al., 1996). Ul6a sp. biofiltershave been successfully integrated into a number of other experimental and commer-cial mariculture systems, efficiently removing dissolved inorganic nitrogen from theeffluent water (Ryther et al., 1975; Tenore, 1976; Vandermeulen and Gordin, 1990;Hirata and Kohirata, 1993). While reported as being effective in its application asa biofilter, particularly in land-based systems, the produced biomass of Ul6a sp. hasbeen of limited commercial value (Kissil et al., 1992; Arieli et al., 1993). Thevaluable rhodophyte Gracilaria sp. has also been cultured in mariculture biofiltersin Eilat and elsewhere (Ryther et al., 1975; Neori, 1991; Buschmann et al., 1994).

One proposed way of increasing the economic viability of seaweed biofilters hasbeen to feed the biomass produced to commercially valuable macroalgivores,particularly abalone (Tenore, 1976). H. tuberculata was introduced for this purposein Eilat (Shpigel et al., 1996). Subsequent feeding trials revealed that H. tuberculatadisplayed improved growth performance when fed a diet of Ul6a sp. supplementedwith 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

217A. Neori et al. : Aquacultural Engineering 17 (1998) 215239

Shpigel and Neori (1996), as the simplest of several combinations of progressivecomplexity. The proposed pilot-scale, two-organism, abalone-seaweed system wassubsequently constructed at the NCM as a first step toward ultimately developinga polyculture system for four organisms (seaweed, abalone, fish and clams). Theperformance of the simple two-organism system, with regard to abalone growthparameters 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 costlycomponent of diets used in aquaculture is protein, which also is a major determi-nant 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 aremajor anticipated benefits of the proposed polyculture concept. N-budget was,therefore, selected as the optimal measurement criterion for this aspect of theexperimental system.

2. Materials and methods

2.1. Organisms

Haliotis tuberculata were introduced into land-based facilities at the NCM fromGuernsey, UK, in 1993 (Shpigel et al., 1996). Ul6a lactuca L. was produced fromvegetative thalli isolated from the Red Sea and cultured in biofilters (Vandermeulenand Gordin, 1990). Gracilaria conferta cultured in the second biofilter had beencollected 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 diagrammedin Shpigel and Neori (1996). The experimental system was designed to allow anevaluation of the biological-chemical practicality of the abalone-seaweed integratedculture concept, not specifically to maximize performance. Therefore, a largemargin of error was allowed, by using low stocking densities of the animals andrelatively large seaweed biofilters. The sizes of the abalone and the seaweed culturevessels were adjusted with the following considerations:

1. A low abalone density (far below the 35 kg:m3 found practical in our regularabalone 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 m2 week1;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 theireffluents 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


abalone while allowing faeces and detritus to drain from the tank; water wasdrained via a removable, 40-mm ID, 60-cm tall stand-pipe, fitted to a hole at thebottom and covered by a 5-mm mesh at the top. Two perforated horizontalaeration tubes on the bottom below the screen kept food algae in suspension. Eight160-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 availablefor abalone attachment. The abalone tanks were each initially stocked with 235 H.tuberculata of 3060-mm shell length (4.132.6 g wet weight) with a total biomassof 2.2 kg (Table 1).

Two seaweed biofilters, identical to those reported in Neori et al., (1996), wereinstalled, one stocked with U. lactuca and the other with G. conferta. They weremade of round-bottom elongated (31.1 m) fiberglass tanks, bottom-aerated andwith a useable water volume of approximately 1500 l. U. lactuca and G. confertawere stocked at 1.5 kg and 12.0 kg m2 (fresh weight) respectively, following therecommendations of Neori (1991) and Neori et al. (1991). The only nutrient sourcefor the whole system was mineral fertilizer (solutions of ammonium sulfate anddisodium phosphate), supplied directly to both biofilters by continuous dripping.The N supply rate was initially about 5.6 g N m2 day1. This ammonia-N fluxwas estimated to provide an optimal combination of good seaweed growth, about50% removal of ammonia-N and a moderate N-content in the seaweed (Cohen andNeori, 1991; Neori et al., 1991). From July 1995 onward ammonia-N was suppliedto the seaweed at only about 4.0 g m2 day1, in an effort to improve the fractionof N removed by the biofilters. The influx of orthophosphate was maintainedthroughout the year at 0.6 g P m2 day1. In addition, the U. lactuca biofilterreceived the entire effluents from abalone tank A and the G. conferta biofilter fromabalone tank B.

2.3. System monitoring

The integrated culture system was monitored for 1 year, beginning in March1995.

2.3.1. AbaloneAt 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 toremove excess water from the mantle cavity) and shell length measured at 23-month intervals. Length is not a particularly useful growth parameter in abalone. Itwas measured and presented below only to allow the readers comparison withprevious studies were weight was not used. The tagged abalone were assumed toconstitute a sub-sample representative of the tank population. Wet weight figureswere 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)


Tab

le1

Bas

icin

form

atio

non

the

abal

one

cult

ure

tank

san

dse

awee

dfr

esh-

wei

ght

yiel

din

two

biofi

lter

tank

s

Sam

plin

gda

te

Tan

kB

Tan

kA

Apr

il19

95Ju

ne19

95Ja

nuar

y19

96A

pril

1995

Mar

ch19

96Ju

ne19

95A

ugus

t19

95Ja

nuar

y19

96M

arch

1996

525

520

1075

531

508

833

Wat

erflo

w78

751

010

67ra

te(l

h1)

Aba

lone

8.96

2.28

4.06

Stan

ding

8.5

2.67

8.91

4.62

5.16

8.34

stoc

k(k

g)33

215

020

331

555

217

0G

row

th(m

g51

728

639

2N

:tan

k:d)

Aba

lone

rest

ocki

ngA

pril

1995

May

1995

June

1995

Oct

ober

1995

Dat

eA

pril

1995

May

1995

June

1995

Oct

ober

1995

235

100

8027

659

1In

divi

dual

s23

510

080

2.19

Kilo

gram

s0.

482.

300.

772.

170.

470.

934.

52

Ani

mal

sw

ere

adde

dbe

fore

sam

plin

gda

tes.


where W0 is the wet weight of an animal at the beginning of each monitoringinterval 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 estimatedfor each day of intensive sampling by Eq. (2).

DB (B0SGR%:100)Mw (g:d, fw) (2)

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

2.3.2. Algal production and abalone feedingAbalone 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 timesthe weight of corresponding abalone biomass, maintained by supplying additionalseaweed every 23 d), to provide good shade for the animals as well as to ensurethat food was continuously available. The experiment was interrupted for 2 monthsfollowing the November 22nd 1995 earthquake in the Gulf of Aqaba; however, theanimals were fed seaweed from other tanks and the monitoring of the animalscontinued.

Table 2Seaweed fresh-weight yield (g:m2:d) in two biofilter tanks in 1995 and 1996

Gracilaria confertaUl6a lactucaDate

210 46Late April 1995403Early May 1995 261

268May-June 1995 286412Late June 1995 Early Junelate July 1995 170

194Early July 1995295Late July 1995 303Late August 1995 57

34284September-October 1995196Late October 1995

14October-November 1995 155168Mid-November 1995 330

81Mid-January 1996 3952Late January 1996 11

197104Early February 199685February-March 1996 136

Mid-March 1996 95 Late March 1996 402


Biofilters were drained every 2 weeks, the seaweed weighed and re-stocked at theoriginal weight. The net yield of algae, including weight of algae harvested forfeeding, was used to calculate the mean daily seaweed production for each 2-weekperiod.

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 thebottom and the screen above was flushed and cleaned from the bottom; deadanimals were removed and their shell length measured; uneaten algae were removedand weighed; the quantity of algae ingested was determined by difference from thetotal weight fed.

Ingestion rate was estimated by dividing the seaweed weight, ingested during thetime interval between two weighings, and the mean abalone biomass for thatinterval (estimated using SGR% and initial abalone biomass measurements for thatinterval).

Food conversion ratio (FCR) was determined by the fresh weight of ingestedseaweed divided by the abalone biomass gain over the same time interval. Algalgrowth inside the abalone tanks, and consequent possible nutrient recycling in situ,was not assessed, hence the estimates of ingestion rate and food conversion ratioare considered apparent.

Annual values of SGR% and FCR were calculated by the sums of ingestedseaweed and abalone growth, adjusted for mortalities and animal stocking.

2.3.3. Nutrient analysesSixteen individuals of H. tuberculata grown under conditions similar to those

described above were sampled at 3-month intervals during 1994; individual wetweight 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 wasdetermined by the Kjeldahl method. Fifteen samples of both seaweed species weretaken between April 1994 and April 1996 and treated in the same way as theabalone samples. The mean nitrogen content of the animals and DB were used toestimate the amount of nitrogen incorporated into abalone tissue during anyspecific 24-h period. Similarly, nitrogen incorporation into algal tissue was deter-mined as the mean tissue nitrogen contentmean daily production.

The form, quantity and diurnal fluctuation of nitrogen and phosphorous flowinginto and out of each tank were determined at approximately 2-month intervals byintensive sampling days from one morning (08:30) to the next (P was analyzed inonly about half of the days). Each such day was divided to four 6-h samplingperiods. Each water sample from a tank was collected during the entire 6-h periodin a separate covered 20-l PVC container via a drip siphon from the effluentstand-pipe. The collected water, typically 5 l, was sub-sampled for analysis. Allsampling and storage vessels for the sampling were pre-soaked for 24 h in 1.0 NHCl and then rinsed well with de-ionized water.

Total nitrogen (TN) and total phosphorous (TP) were analyzed by a TechniconAutoanalyzer II using standard methods and following the modified persulphateoxidation procedure as described by Neori et al. (1996). Total dissolved nitrogen


and phosphorous (TDN and TDP) were analyzed similarly, only following filtrationthrough acid-washed Whatman GF:C filters. Sub-samples of these filtrates weredeep-frozen, for subsequent determination of the mineral forms of N (DIN) and Pby standard Autoanalyzer methods (Krom et al., 1985). Suspended particulatenitrogen (PN) was determined by the difference between TN and TDN, anddissolved organic nitrogen (DON) was estimated by subtracting DIN from TDN.Flowmeter readings were used to determine mean flow rate of water through thetanks during each sample day (Table 1). Water flow and nutrient concentrationwere used to determine the overall rate of input and output of nutrients for eachtank and biofilter. Net abalone production of N and P and their net uptake by thebiofilters were calculated as the difference between absolute levels entering andleaving each tank.

Complete system nitrogen budgets were constructed for each 24-h samplingperiod with the absolute nitrogen quantities, according to the scheme in Fig. 1.Nitrogen partitioning was also standardized by biofilter water surface area orabalone biomass to give comparable nitrogen budgets for the biofilters and abalonetanks separately.

3. Results

3.1. Temperature

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

3.2. Abalone performance

Initial abalone growth rates differed between the two tanks, but convergedduring AprilMay 1995 to subsequently follow similar patterns. The best growth(both SGR% and shell length) occurred in the spring, and it progressively declinedtowards an autumn minimum (Fig. 3). By February 1996 growth rate had begun toincrease. Over 1 year, the tagged animals grew with an average SGR% of 0.26290.033%:d (n28) in tank A and 0.25190.037%:d (n31) in tank B.

FCR values (Fig. 4) were low (i.e. efficient) and relatively stable during thespring, but increased (i.e. became less efficient) in summer to maxima in October of4093.3 in tank A and 2992.5 in tank B. Annual FCRs of 20 and 17 werecalculated for the two abalone tanks, using the overall growth (corrected formortalities 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 mortalitydecreased 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.


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


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

However, the interpretability of these annual figures in relation to Fig. 5 iscompromised by the periodic restocking of the tanks, as reported in Table 1. Thehigh mortality rates in the early months are offset in the overall annual rate by thelarger animal numbers later. The dead animals were generally found in areas wherethe abalone tended to crowd, notably in the darkest corners of the tank; aggressivebehaviour, the use of the radula to inflict foot lesions on conspecifics, was observedwithin these stacks.

3.3. Algal production

Production of Ul6a lactuca was seasonally-dependent (Table 2). Production waslower in winter than in the rest of the year, averaging 29295 g fresh weight m2

d1 (5291 g dry weight m2 d1) in the summer, and 8399 g fresh weight m2

d1 (1591 g dry weight m2 d1) in winter. Production rates in the spring andautumn showed greater variability; annual maximum and minimum values of 412 gfresh weight m2 d1 and 52 g fresh weight m2 d1 were recorded. Gracilariaconferta yield was erratic and consistently lower than U. lactuca (Table 2). Algalstocks within the G. conferta biofilter repeatedly crashed during the monitoringperiod. A cessation in net growth was followed by frond fragmentation andwashout, and then a take over by opportunistic chlorophytes, predominantly Ul6aspp. and Enteromorpha spp (see also in Friedlander et al., 1987, 1991; Ugarte andSantelices, 1992; Buschmann et al., 1994). When production could be sustained, inAprilJune 1995, it averaged 231931 g fresh weight m2 d1.


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

3.4. Nitrogen partitioning

3.4.1. Abalone tanksMean N content of abalone was 1.6490.07% of wet weight (12.0290.09% of

soft tissue dry weight), in U. lactuca 0.8190.05% of wet tissue (4.690.1% of dryweight) and in G. conferta 0.8190.06% in wet tissue (5.890.26% 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 intoaccount in the abalone growth figures) and seaweed protein. Each abalone tankreceived seaweed biomass from the biofilters downstream. Overall, the A abalonetank 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 therest 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.


Tab

le3

Dai

lyN

budg

ets

for

abal

one

tank

sA

and

Bon

date

sof

inte

nsiv

esa

mpl

ing

duri

ng19

95

1996

.Fig

ures

repr

esen

tbi

omas

s-sp

ecifi

cra

tes

(mic

rogr

amN

:gab

alon

e:d

),an

dth

eco

rres

pond

ing

perc

enta

ges

rela

tive

toth

eto

tal

Nin

put

toth

eta

nk

Tan

kA

Tan

kB

Mar

ch19

96A

pril

1995

June

1995

Janu

ary

1996

Mar

ch19

96A

vera

geSD

Janu

ary

1996

Dat

e:A

ugus

t19

95Ju

ne19

95A

pril

1995

NIn

puts

00

00

00

0In

flow

ing

wat

er0

00

245

536

430

394

237

536

382

103

356

394

310

Ul6

ala

ctuc

a10

010

071

6410

010

081

1870

5864

%of

inpu

tto

tal

017

522

40

00

112

281

106

176

Gra

cila

ria

conf

erta

150

00

2936

00

1918

3042

36%

ofin

put

tota

l53

660

561

823

753

649

4N

inpu

tto

tal

146

506

675

486

245

100

100

100

100

100

100

100

010

0%

ofin

put

tota

l10

010

0

NO

utpu

tsA

balo

negr

owth

3766

5037

6262

3214

762

3362

711

816

1225

148

%of

inpu

tto

tal

79

2918

742

314

714

112

552

828

416

124

955

420

2E

fflue

nts

7924

2353

9959

%of

inpu

tto

tal

2549

8242

7646

021

319

116

259

024

934

639

616

5N

outp

utto

tal

235

616

102

8635

3169

110

7227

7891

48%

ofin

put

tota

l

76

39

2

427

74

54

148

161

Defi

cit

(out

-in)

11

0

59

251

4

14

65

69

3110

28

227

9

22

52

%of

inpu

tto

tal

avg.

sum

Aba

lone

grow

th33

215

020

331

555

229

1832

4T

otal

,m

gN

:tan

k13

539

228

617

051

7

Seaw

eed

inpu

t20

4348

0313

7925

0920

1047

7624

498

2722

1222

1351

3119

2508

Tot

al,

mg

N:t

ank


Fig. 4. (a) Mean ingestion rates and (b) calculated food conversion ratios (FCR, fresh weight of algaeingested: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 feedingactivity of the animals (metabolic by-products, undigested material and algal cellcontents not ingested), as negligible quantities of N came in with the fresh seawater(Table 3). The nitrogen supplied as seaweed protein was either incorporated intoabalone biomass, washed out of the abalone tank into the biofilter or wasunaccounted for (deficit). During most of the days monitored, much of the Nentering the abalone tanks (up to 69%) remained unaccounted for, whereas on twooccasions N surpluses of 2% and 10% were measured (Table 3). On average, of theN that entered the abalone tanks only 1498% was incorporated into abalonebiomass over the entire monitoring period. Of the rest of the N that entered theabalone tanks, 59925% flowed out into the seaweed biofilters with the effluent and28927% was not found (Table 3).

Total N in the abalone effluents averaged for the entire nine intensive samplingdata sets (five for tank A and four for tank B) was 301973 mg N:g abalone:d(Tables 3 and 4). This TN value was comprised of ammonia-N (62912 mg N:gabalone:d), DON (145963 mg N:g abalone:d), and PN (101955 mg N:g abalone:d). The production rate of TN and its components did not show discernible


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

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

3.4.2. Seaweed biofiltersSmaller 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 daysmonitored, incorporated larger fractions of the N entering the biofilter into seaweed

Table 4Quantity and forms of nitrogen production measured in abalone tank effluent water during 6 hsections of 24 h monitoring periods; figures represent mean microgram N:g abalone biomass, producedduring 6 h (9S.E.; 5 dates in tank A and 4 dates in tank B)

Sample period:Form of N in abaloneeffluent:

20:3002:30 02:3008:30 Total:d08:3014:30 14:3020:30

19 (914) 14 (911) 62 (912)Ammonia-N 18 (911) 11 (911)38 (946) 52 (9101)Dissolved organic N 26 (944) 26 (927) 145 (963)9.3 (915) 101 (955)23 (926) 37 (986)31 (951)Particulate N

65 (949)91 (997)64 (938)Total N 78 (983) 301 (973)


Tab

le5

Dai

lyN

budg

ets

for

biofi

lter

tank

sst

ocke

dw

ith

Ul6

ala

ctuc

aan

dG

raci

lari

aco

nfer

taon

date

sof

inte

nsiv

esa

mpl

ing

duri

ng19

95

1996

.F

igur

esre

pres

ent

for

each

tank

area

-spe

cific

rate

s(m

gN

:m2

ofbi

ofilt

erta

nk:d

),an

dth

eco

rres

pond

ing

perc

enta

ges

rela

tive

toth

eto

tal

Nin

put

toth

eta

nk

Ul6

aG

raci

lari

a

Mar

ch19

96A

pril

1995

June

1995

Janu

ary

1996

Mar

ch19

96D

ate:

Apr

il19

95Ju

ne19

95A

ugus

t19

95Ja

nuar

y19

96

Inpu

ts52

012

6311

119

135

515

6822

185

3F

rom

abal

one

tank

348 8

1124

23

828

4%

ofin

put

tota

l13

4038

5632

5578

4038

4038

4038

5578

4038

Add

ednu

trie

nts

5632

8976

9897

9272

9687

92%

ofin

put

tota

l45

5853

0157

4357

6943

9356

0658

5364

3143

86N

-inp

ut-t

otal

100

100

100

100

100

100

%of

inpu

tto

tal

100

100

100

Out

puts

3231

130

1365

1587

083

4A

lgal

harv

est

2437

3316

1687

1861

224

360

2952

56%

ofin

put

tota

l30

4913

7068

631

2254

19E

fflue

nts

3107

2619

1505

2649

5824

1271

9758

%of

inpu

tto

tal

3441

5334

8362

8015

0020

5147

0954

1947

9459

3539

42N

-out

put

Tot

al90

7611

826

3610

797

%of

inpu

tto

tal

8292

979

42

43

3718

316

44

4

187

49

6

1059

10

75D

efici

t(o

ut-i

n)

2418

74

64

7

3

18

8

10%

ofin

put

tota

l

4759

6642

4276

8829

3F

iltra

tion

effic

ienc

yin

biofi

lter

s(%

ofin

put

tota

l)


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

SE % of N inputmgN:m2:d

1004734 779Input

Outputs2.244105Abalone growth

SeaweedTotal harvest 1139 341621

19394Fed to animals within the system 878Unused (export) 16743

552614Effluents 1293

1273 27Deficit (out-in)

production than did G. conferta (Table 5). Overall, nitrogen filtration efficiency ofthe biofilters was highest in summer (Table 5). Although the G. conferta biofilteroccasionally removed N more efficiently than the U. lactuca biofilter, it incorpo-rated a smaller fraction of N into a harvestable biomass and created largerN-deficits. Generally, the U. lactuca tank removed 58% of the N input to thesystem, 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 ofinorganic N that supplied large fractions of unaccounted-for N were associatedwith visual observations of frond fragmentation in this seaweed.

Most of the N budget was comprised of ammonia, the inorganic form suppliedto the biofilters, and the other N forms were inconsequential. DON and PN (datanot shown) were sometimes removed and sometimes produced in the biofilters, butin small quantities (B10% of the overall N budget). Oxidized N (data not shown)was sporadically produced in both biofilters in small quantities (up to 5% of theoverall N budget).

3.4.3. O6erall N budgetsIn 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 assimilatedabout 12% of the seaweed given to them, and therefore only 2.2% of the total Nsupplied was harvested as abalone biomass.

There was, however, a large net seaweed surplus, about half of the overallproduction of algae in both biofilters. Nearly twice as much surplus was producedby U. lactuca than by G. conferta. About half of the N input of the entire four-tanksystem was released in the effluents, and about a quarter of the N was unaccountedfor (deficit). The deficit N (which possibly was also released) within G. confertabiofilter was greater than in the U. lactuca biofilter.


3.4.4. PhosphorousNo phosphorous was detected in the influent or effluent water of either abalone

tank. The biofilters (data not shown) both consistently removed less than 25% ofthe phosphorous added (with the exception of the G. conferta in January 1996, thatremoved 84.8% of phosphorous encountered over 24 h).

4. Discussion

The concept of ecological sustainability in aquaculture refers to the maximizationof internal feedback (e.g., recycling) within a culture system. This minimizes theinputs and the wasted outputs of resources (Dalsgaard et al., 1995), such asnutrients, water and energy, in effluent water. The results presented here show thepotential of the integrated abalone-seaweed culture to be practical. A quantitativeevaluation of the performance of each component of the system studied here willaid in the development and design of more practical facilities and techniques forintegrated mariculture, based on internal nutrient recycling and leading to bettereffluent quality. The system incorporates a number of features that can increase theecological sustainability of the proposed integrated culture system, as follows: (a)the use of the same water for both abalone and seaweed cultures reduces seawaterrequirements by half in this first trial; (b) biofiltration and recycling of the abalonenutrient excretions by the seaweed reduces both the nutrient input requirements andthe overall environmental impact of the culture operation; (c) the use of biofilter-grown seaweed eliminates the need for a destructive harvest of natural seaweedbeds; and (d) the chemical composition of the cultured seaweed, and hence theirnutritional value to the algivores, is controllable.

Following refinements to the integrated culture system that can arise from thepresent results, the incorporation of fish and bivalves will follow, according to theprinciples 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 watertemperatures corresponded closely to the summer temperatures considered optimalfor growth in the Ormers natural range (Hayashi, 1982; Clavier and Richard,1986). The initial differences observed in SGR% between the two abalone popula-tions may be explained by differences in the timing of spawning, usually syn-chronous within a confined abalone population (A. Marshall, NCM, Israel,personal communication).

From May to October, when daytime water temperatures in Eilat remainedabove 23.5C, growth rates of the Ormer were low, reflected by increased FCRs. Ithas been suggested (Shpigel et al., 1996) that the elevated temperatures increasebasal metabolic rate, thus reducing the energy available for somatic growth.


Ingestion rates remained fairly constant throughout the year, in close agreementwith rates recorded by Mercer et al. (1993). They reported 59% daily body weightfood ingestion by H. tuberculata fed U. lactuca, suggesting that the animals in thepresent 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 inEilat (Shpigel et al., 1996). Elsewhere, for H. tuberculata of similar size rangesgrown in warm water culture (1820.5C), growth rates of 1520.3 mm year1

were recorded (Forster, 1967; Hayashi, 1980, 1982; Mgaya and Mercer, 1995). In aparallel experiment H. tuberculata from the same stock as used in the present studyshowed growth rates corresponding to 21.892.7 mm year1, in a controlledaquarium environment (Ragg et al., unpublished data). In the present studyabalone were stocked at densities (maximum 166 individuals m2) well below thelevels 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 presentstudy allowed animals to move freely, hence the abalone, responding to the samestimuli, such as negative phototaxis (Mgaya and Mercer, 1994), and their gregari-ous nature (Douros, 1987) tended to crowd. This apparently induced local effects ofsevere 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 improvinggrowth performance, mean annual SGR%s and FCRs were better here than theconservative estimates proposed by Shpigel and Neori (1996) (Table 7) andconcurred with those found by Mercer et al. (1993).

Smothering and aggressive behaviour between conspecifics are held partly re-sponsible for observed abalone mortality, and initial high mortality is likely to beassociated 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, thegrowth rate of U. lactuca appearing to be predominantly dependent upon watertemperature and light, in agreement with the findings of Vandermeulen and Gordin(1990), Israel et al. (1995) and Neori et al. (1996). Constant daily yields accompa-nied the more stable water temperatures during winter and mid-summer, withproduction levels comparable to those of U. lactuca grown in other biofilters (Neoriet al., 1991, 1996) and using artificial inorganic nitrogen and phosphorous sources(DeBusk et al., 1986; Israel et al., 1995). The annual mean seaweed production of230 g fresh weight (42 g dw) m2 d1 obtained here exceeds that of almost allknown intensive terrestrial and marine plant cultures (Lapointe et al., 1976).

Gracilaria spp. is highly sensitive to temperature (Edding et al., 1987; Friedlanderet al., 1987, 1991; Levy and Friedlander, 1990; Ugarte and Santelices, 1992);optimum growth of G. conferta occurs in cultures of 2026C (Levy and Friedlan-


Tab

le7

Com

pari

son

betw

een

the

yiel

ds,

and

corr

espo

ndin

gsy

stem

dim

ensi

ons,

pred

icte

dfo

ran

inte

grat

edH

.tu

berc

ulat

a:U

.la

ctuc

asy

stem

per

kgof

nitr

ogen

inpu

t,us

ing

the

figur

espr

opos

edby

Shpi

gel

and

Neo

ri(1

996)

and

the

mea

nan

nual

yiel

dsfo

und

poss

ible

inth

epr

esen

tst

udy

Ass

umpt

ions

Ass

umpt

ions

Cal

cula

ted

from

mea

nva

lues

Pre

dict

edby

Shpi

gel

and

Neo

ri(1

996)

foun

din

the

pres

ent

stud

y

Rec

eive

sa

net

N-fl

uxof

4g

6554

.9R

emov

es55

%of

amm

onia

-NY

ield

ofU

l6a

lact

uca

(kg

m

2d

1;

yiel

d0.

23kg

m

2at

flux

of4

gm

2

d1;

yiel

dfr

esh

wei

ght

d1):

kgN

d1

0.25

kgm

2

d1

adde

dto

syst

emB

iofil

ter

surf

ace

area

requ

ired

239

m2

U.

lact

uca

yiel

dof

0.23

kgm

25

0m

2U

.la

ctuc

ayi

eld

of0.

25kg

2d

1m

2

d1

tosu

ppor

tth

ispr

oduc

tion

FC

R

252.

72.

6F

CR

20

Yie

ldof

abal

one

(kg

fres

hw

eigh

td

1):

kgN

adde

dto

syst

emSG

R

0.3%

d1;

stoc

ked

at25

.7m

325

m3

Vol

ume

ofw

ater

requ

ired

toSG

R

0.3%

d1;

stoc

ked

atsu

ppor

tth

ispr

oduc

tion

of35

kgm

3

35kg

m

3

abal

one


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 bysummer and winter temperature extremes, as well as large diurnal ranges, combinedwith the continuous presence of nutrients, favouring the development of foulingchlorophytes, were responsible for the poor performance of G. conferta in thepresent study.

4.3. Nutrient partitioning

4.3.1. Abalone tanksOn 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 aswe had reported for marine fish in intensive fishponds (Krom and Neori, 1989) andintegrated 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 largeproportion of the nitrogen remained unaccounted for. These deficits are attributedto 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-to-

day 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, andalso light and temperature (Friedlander et al., 1987; Vandermeulen and Gordin,1990; Cohen and Neori, 1991; Pedersen, 1994). In the present study, average valueswere used to represent the nitrogen content of either algal species throughout themonitoring period, hence no accommodation was made for possible variations inthe amount of nitrogen within food algae or the subsequent uptake or loss ofnitrogen by the algae within the abalone vessels.

4. Tightly-coupled nitrification-denitrification in animal digestive tract, faeces orin corners of the rectangular vessels. Such efficient coupling that leads to thecomplete removal of the oxidized N as soon as it is produced has been known forhighly organic flooded soils and sediments (Reddy and Patrick, 1984). It couldexplain both the absolute lack of oxidized N in the abalone tanks (as opposed toits sporadic detection in the waters of the seaweed tanks) and the large N-deficitthere.

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 formationof 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 thatthe amount of nutrients lost during the weekly cleaning of the tanks was muchmore than we assessed.


Diurnal variation in composition of nitrogenous abalone effluent was on averagelimited to ammonia, most probably a net result of periods of greatest abaloneactivity (Barkai and Griffiths, 1987; Peck et al., 1987; Fleming et al., 1996) on theone hand, and daylight uptake of ammonia by the uneaten seaweed (Cohen andNeori, 1991) on the other hand. Un-ingested algal cell contents liberated by abaloneradula scraping action may account for the persistently high presence of DON andPN in tank effluents. Average ammonia production rate of 62 mg N:live g:d in thepresent study appear higher than the 36 mg N:live g:d, which can be calculated fora 9.3-g (4 g dw) animal by the equation given in Peck et al. (1987):

ln U0.656 ln W0.914 (3)

Uammonia excretion in mmol N:h and Wdw of whole animal. This is notsurprising, considering the markedly higher temperatures in our study.

4.3.2. Seaweed biofiltersThe U. lactuca biofilter showed consistent performance throughout the year and

most of the nitrogen removed in this biofilter was accounted for by subsequentgains in algal biomass. Biofiltration efficiency was highest in summer, correspond-ing to fastest U. lactuca growth. The filter removed approximately half of thenitrogen, encountered predominantly as ammonia-N, at an even rate over 24 h, asnoted by Vandermeulen and Gordin (1990) and by Cohen and Neori (1991). Theconsistent biofiltration performance of U. lactuca is highlighted when comparingthe present nitrogen removal efficiencies to those recorded by Cohen and Neori(1991) who, working at the same site, found mean removal rates of 4956% ofammonia-N supplied at fluxes of 4.85.2 g m2 d1. Cohen and Neori (1991) alsodemonstrated that nitrogen filtration efficiency was enhanced as influent nitrogenflux decreased; however, there was a corresponding reduction in U. lactuca tissuenitrogen, 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 hasalso been noted in other seaweed biofilters (DeBoer et al., 1978; Neori et al., 1996).Macroalgae grown in artificially enriched media are typically supplied with inor-ganic nitrogen and phosphorous at molar ratios of 1013:1, N:P (Vandermeulenand Gordin, 1990; Friedlander et al., 1991; Ugarte and Santelices, 1992; Israel etal., 1995). In the present system, inorganic nutrients were added in accordance withthe higher Redfield ratio for phytoplankton cells, N:P16:1. Despite this elevatedratio, phosphorous removal efficiency was low.

In the G. conferta biofilter, high nitrogen filtration efficiencies in spring 1995could not be accounted for by a correspondingly high production of Gracilariatissue. It is considered likely that nitrogen was removed from the water byautotrophic fouling organisms; apart from the visibly obvious presence of macro-scopic chlorophytes, small quantities of oxidized nitrogen were frequently detectedin the effluents of this tank. It is therefore possible that there, the same nitrification-denitrification coupled processes competed with the G. conferta for ammonia, asfound by Dvir (1995), and created large N-deficits. Gracilaria conferta has always


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. lactucaculture.

In both biofilters a large proportion of the nitrogen supplied was removed assurplus 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 studymake it possible to determine a more appropriate ratio and estimate the subsequentsystem productivity.

Owing to the unreliable performance of the G. conferta biofilter, the followingcalculations are based on integrated abalone:Ul6a tanks, stocked with animals ofthe size range used here, typical of second-year growout H. tuberculata (Mgaya andMercer, 1994). Assuming a steady annual ingestion rate of 5.9% body weight d1,and mean U. lactuca production of 230 g m2 d1 (49% N-filtration efficiency,58% if N-recycling is excluded), and using the more conservative parameters of theabalone population from tank A (mean FCR20; 45% of N entering the abalonetank is released in tank effluents), an appropriately proportioned system can beproposed. The productivity of such a system, standardized to 1 kg N input, iscompared to the original model of Shpigel and Neori (1996) in Table 7. Theperformance of the experimental system studied here shows close agreement withthe predicted models.

This comparison provides also an indication of the benefits of the integration ofseaweed and abalone culture units into a single system. If the U. lactuca andabalone were grown in separate systems, seawater supply would be doubled, thenitrogen leaving the abalone vessel would be dumped into the sea and a corre-sponding amount of nitrogen (up to 24% in the 27 March 1996 experiment) wouldhave to be added to the U. lactuca culture. Hence, using this example, separatingthe culture units would result in the need to supply an additional 24% nitrogen tothe algal unit and a similar (all the abalone effluents N) increase in nitrogen releaseto 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 calculatethe 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 sufficientproduction during minimum winter growth (mean 82 g Ul6a m2 d1), this wouldrequire a filter 2.8 times larger than proposed by the model. A more practicalsolution would be to introduce a second U. lactuca biofilter in series, to serve as apolishing filter, further reducing nutrient loading in system effluents, as successfullyapplied by Lapointe et al. (1976), Krom et al. (1995) and Neori et al. (1996); thesecond filter would also provide an additional source of U. lactuca biomass if theproduction from the first filter fails to meet demands.

The level of inorganic nitrogen and N:P necessary to produce U. lactuca ofoptimum nutritional value, while minimizing the level of nutrients in the effluent,still needs to be determined and corrected for nitrogen supplied by abalone


effluents. The commercial application of such a system would also benefit from theuse of an improved abalone vessel design that does not permit excessive freemovement of animals and subsequent crowding problems, as recommended byFleming 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 algaebiofilter area to kilogram of cultured abalone. Supplying ammonia-N influx atdouble 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 toreduce 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 begrown in a separate temperature regulated culture, receiving weekly nutrient pulses.This can further reduce the area of seaweed biofilter per kilogram of rearedabalone.

Acknowledgements

The authors would like to offer special thanks to A. Marshall for valuableobservations as system manager; our gratitude also to D. Ben-Ezra, R. Fridmanand 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. Gold-berg for critical reviews of the manuscript. The project was supported by the IsraeliMinistry for Energy and Infrastructure and by a joint program of the EC and theIsraeli Ministry for Science (Grant No. 4564192 to M.S. and A.N.).

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