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quacultureELSEVIER Aquaculture 130 (1995) 351-360

Effects of silage preservation on astaxanthin formsand fatty acid profiles of processed shrimp

(Pandalus borealis) wasteAlain Guillou**, Michel Khalil, Lucien Adambounoub

Dkpartement dOct%znographie et Centre Oceanographique de Rimouski, Universiti du QueYbec ci Rimouski(UQAR), 310 allie des Ursulines, Rimouski, Qut . G5L 3A1, Canada

bD6partement de Biologic et des Sciences de la santeet Centre OcPanographique de Rimouski (COR),Universite du QuPbec d Rimouski (UQAR), Rimouski, Qut . GSL 3A1, Canada

Accepted 12 September 1994

bstract

Acid silage of shellfish processing waste has been reported to be a good and economical techniqueto protect these biomasses from bacterial decomposition. Shrimp Pundulus borealis) by-productscontain some value-added nutrients for the aquaculture industry such as carotenoid pigments (mainlyastaxanthin) and n-3 polyunsaturated fatty acids. The aim of this work was to determine the effect ofensiling shrimp waste during a long period of time (more than 3 months) on some unstable compo-nents such as the astaxanthin forms (free, mono- and diesterified) and polyunsaturated fatty acids.Comparisons of astaxanthin forms and the fatty acid profiles were performed on defrosted shrimpwaste and on a 14-week-old shrimp waste silage. No significant difference (P20.05) in the totallipids extracted from the two forms of shrimp waste was observed. Nevertheless, a small quantity ofthe red pigment, presumably an astaxanthin portion, was observed to stay firmly bound to the shrimpcarapace after the solvent extraction in shrimp waste compared to the full recovery obtained in ensiledshrimp waste. This may explain the significantly (P < 0.05) higher concentration of total astaxanthin(4.57 vs 3.99 mg/g) found in the crude oil extracted from shrimp waste silage. Higher percentages(P < 0.01) of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) were found in ester-ified astaxanthin from shrimp waste silage (43.9% and 45.5%) in comparison with their shrimp waste(24.7% and 20.3%) counterparts. This suggests that EPA and DHA are the principal fatty acidsesterified with the portion of astaxanthin linked to chitin in the shrimp carapace. The utilization ofshrimp waste silage as a pigmenting component of salmonid feeds is also discussed.Kqywords: Silage; Shrimp waste; Astaxanthin forms; Fats and fatty compounds; Feeding and nutrition - fish,pigmentation

Corresponding author. Tel. ( + l-418) 724-1770 or 724-1608; Fax ( + 1-418) 724-1842.0044-8486/95/$09.50 0 1995 Elsevier Science B.V. All rights reservedSSDIOO44-8486(94)00324-6


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1 Introduction

It is well known that the pink to red colouration of the flesh of wild salmonids is due tocarotenoid pigments, mainly astaxanthin (Ax) of dietary origin (Khare et al., 1973; Kita-hara, 1984; Schiedt et al., 1986; Scalia et al., 1989a). Pigmentation of farmed salmonids isof economic importance for the salmon industry (Torrissen et al., 1989). The naturalpigmentation of farmed fish can be achieved principally by the inclusion in the diet ofsynthetic Ax (Foss et al., 1987; Storebakken et al., 1987; Choubert and Storebakken, 1989)or with Ax from crustacean sources (Saito and Regier, 197 1; Spinelli and Mahnken, 1978;Arai et al., 1987).

The northern shrimp, Pandal us boreal i s, has high concentrations of Ax and good poly-unsaturated fatty acid (PUFA) profiles (Ackman and Eaton, 1967; Lambertsen and Braek-kan, 1971; Johnson, 1992; Shahidi et al., 1992). Thus, the large quantity of processedshrimp waste (SW) produced in Gaspesie coast (Quebec, Canada) could possibly be aneconomic source of natural Ax and PUFAs for pigmented feeds of reared aquatic species.Nevertheless, the high concentrations of chitin and calcium carbonate in SW interfere withabsorption of carotenoids in fish, making them unsuitable as flesh pigmenting sources forsalmonid fishes (Simpson et al., 198 1; Choubert and Luquet, 1983). Ensiling SW in acidresulted in improved uptake of Ax by rainbow trout and Atlantic salmon (Torrissen et al.,1981; Tidemann et al., 1984). Ax is protected against oxidation in shrimp waste silage(SWS) , but a slow conversion of its diester to the corresponding monoester was observedwhen the SWS was stored at 4-X for 21 days (Torrissen et al., 1981).

The aim of this work was to determine the effect of ensiling SW for a long period of time( 14 weeks) on Ax forms (free, mono- and diesterified) and PUFAs from the lipid fractionsof this important shellfish processing waste material.

2. Materials and methodsCarot enoi d and l i pi d source

SW made of cephalothoraxes, digestive glands and shells from boiled northern shrimpproduced in October 1991 by the company Les Crustacts des Monts Inc. (Ste-Anne-des-Monts, Quebec, Canada) was used as the source of carotenoid pigments and fatty acids.The processed SW containing about 20% dry matter was divided into two parts. Five kgwere frozen ( - 30C) in an opaque plastic bag with a minimum air volume for 2 daysbefore extraction procedures, and 10 kg were ensiled immediately.Sil age preparat i on

Ten kg of SW were mixed with 12% (v/w) of 60% sulphuric acid, 6% (v/w) ofconcentrated phosphoric acid and 1% (v/w) of propionic acid (Tidemann et al., 1984). Ablend ( 1: 1, w/w) of butylated hydroxytoluene (BHT) /ethoxyquin (200 mg/kg of SW)was added to the silage to prevent oxidation of carotenoid pigments and fatty acids. ThisSWS was placed in a plastic bucket and stored at 510C for 14 weeks. Every week thesilage was well mixed.


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A. Guillou et al. /Aquaculture 130 (1995) 351-360 353

Carotenoid and lipid extractionsTwo hundred grams of defrosted SW or SWS were placed in 12 Erlenmeyer flasks of 1

liter capacity with 400 ml of acetone containing 200 mg of BHT/l. The flasks were mechan-ically agitated for 16 h in the dark at 4C. The red pigmented solvent was recovered underslight vacuum filtration (filter paper no. 4, Whatman, Clifton, NJ, USA). Fresh acetone(250 ml) was added to the flasks and they were agitated for another 2 h. The solvent phasewas filtered and added to the first fraction. Then 350 ml of light petroleum ether (b.p. 40-60) were added and mixed for 6 h to the samples. The solvent phase was recovered byfiltration. At this stage, all SWS samples showed a complete loss of colouration whereasthe SW samples had a weak orange colour when dried. Acetone and petroleum ether (PE)extracts were concentrated under vacuum (Rotavapor-R; Biichi, Flawil, Switzerland) attemperatures not exeeding 45C. For each sample, acetone and PE fractions were mixed ina separatory funnel and crude lipid extract samples were obtained as described by Choubert( 1977). We picked up, at random, four extracted oil samples from the 12 extractions madefor each treatment and mixed them together to produce our analytical samples (n = 3).

Chemical analysisTotal Ax was determined with a Lambda 3 UV/VIV spectrophotometer (Perkin-Elmer,

Norwalk, CT, USA) set at 473 nm, the maximum absorption spectrum of Ax in PE, or at475 nm, the maximum absorption spectrum of Ax in acetone (Buchwald and Jencks, 1968).Free Ax samples were determined in acetone because solubilization of this Ax form ispoorly achieved in PE. Ax concentrations were calculated by utilizing 2400 and 1910 asextinction coefficients ( E{Tm) of Ax in PE (Meyers and Thibodeaux, 1983) and in acetone(Storebakken et al., 1987)) respectively. Individual carotenoid separations and determina-tions were performed with a series 3B liquid chromatograph (Perkin-Elmer) coupled to aSP 8490 UV-VIS detector (Spectra-Physics, San Jose, CA, USA) using a Cis non-endcap-ped Zorbax ODS (P.N. 884950.543) steel column of 4.6 X 250 mm (ChromatographicSpecialities, Brockville, Ontario, Canada) preceded by a Cis Resolve guard column(Waters, Mississauga, Ontario, Canada). Except for the mobile phase and column ther-moregulation, the isocratic reversed-phase HPLC method was made in accordance withGuillou et al. ( 1993).

The saponification procedure used before HPLC carotenoid determinations was madeaccording to Kimura et al. ( 1990). The crude shrimp oil samples containing Ax and itsesters were purified and condensed by using microcrystalline cellulose according to Inoueet al. ( 1988). Thin-layer chromatographic separation of Ax forms was done as describedby Scalia et al. ( 1989b).

Fatty acid methyl esters (FAMES) were prepared according to AOAC methods ( 1990a)and separated with a Supelcowax-10 capillary column (Supelco, Oakville, Ontario, Canada)using a Sigma 2000 gas chromatograph coupled to a Sigma 15 integrator Perkin-Elmer) .Running temperatures and time parameters were made according to AOAC methods( 1990b). Fatty acids were identified by reference to a standard mixture of commercialFAMES (Sigma, St. Louis, MO, USA). Dry matter was measured by drying fresh samplesat 100C during 48 h, and pH was taken in the press liquid of SWS.


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354 A. Guill ou et al. /Aquaculture 130 1995) 351-360

Statistical analysisThe data were subjected to analysis of variance and students r-test or to a nonparametric

statistical method when the variance of the test groups was abnormal (Snedecor and Coch-ran, 1989). The threshold for rejection of the null hypothesis (~(1 = ~2) was fixed atP10.05.

3. ResultsAstaxanthin forms

The acid mixture used in this experiment produced a SWS with a very low pH ( 1.7) incomparison with some crustacean silages (range from 2.0 to 4.5) produced by other authors(Torrisscn et al., 1981; Chen and Meyers, 1983; Tidemann et al., 1984; Omara-Alwala etal., 1985). No significant differences (P > 0.05) were observed between the percentage ofmoisture and total lipid extracted from SW and SWS. Nevertheless, the crude shrimp oilextracted from SWS was slightly more concentrated (P < 0.05) in total Ax ( 14.5%) thanthe oil obtained from SW (Table 1). The concentration procedure (Inoue et al., 1988) usedon crude shrimp oil extracts made an approximate 3-fold increase in the concentration oftotal Ax but this procedure resulted in similar Ax concentrations between the SW and SWSoil extracts (Table 1) .Table IMoisture. total lipid (90 of we1 weight) and pH in the shrimp waste (SW) and shrimp waste silage (SWS) andtotal astaxanthin (Ax) content (mg/g of oil) of the crude shrimp oil (CSO) and concentrated oil (CO)

SW swsof moisture (n = 8)

oftotallipid(n=6)pH (n=3)Total Ax in CSO (n = 3)Total Ax in CO (n = 3)

79.5 I f 2.2 77.23 f 0.20.77 f 0.06 0.78 f 0.06

N.D. I .70 f 0.023.99f0.16 4.57 f 0.07

12.71 kO.98 12.21 f 0.95Results are expressed as the means f the standard deviations of n determinations.Significantly different P < 0.05).N.D. = not determined.Table 2Free all-tram astaxanthin (A-T-Ax) concentrations (mg/gofoil) determined withareverscd-phase HPLC methodin oil extracted from shrimp waste (SW) and from shrimp waste silage (SWS) after saponification or concentrationprocedures

Saponified oil

SW sws

Concentrated oil

SW sws

A-T-Ax 1.07*0.12 0.32 f 0.04 0.83 f 0.19 0.51*0.13Results are expressed as the means f the standard deviation of triplicate determinations.Significantly different P < 0.05).


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Table 3


Astaxanthin concentrations (mg/kg of wet weight) of shrimp waste (SW) and shrimp waste silage (SWS) andthe relative distribution (in %) of astaxanthin forms (free, mono- and diester)Treatment

SWsws

Total astaxanthin(mg/kg)

30.9 f 1.335.8 f 0.6

% of astaxanthin formsdiester monoester free75.9f2.4 18.5 it 1.0 5.6k2.276.1 f 1.6 20.4* 1.1 3.5 f 0.4

Results are expressed as the means f the standard deviations of triplicate determinations.Significantly different (P < 0.05).Table 4Composition (in % of total) of major fatty acids (FA) of crude shrimp oil (CSO), mono (M) and diester (D)astaxanthin fractions obtained from shrimp waste (SW) and shrimp waste silage (SWS)PA SW sws

cso M D cso M DSaturated12:o 2.8 f 0.514:o 3.9 f 0.416:0 12.5 f0.618:0 1.450.2I: 20.6Monoenoic16:la 9.2+ 1.4lS:ln-9 11.650.3lS:ln-7 6.3kO.l20: 111-9 5.2 f 0.322: 111-9 5.1 f 1.31 37.4Polyenoic18:2n-6 0.7 f 0.0218:3n-3 0.6 f 0.0418:4n-3 0.3 f 0.0320:2n-6 trace20:5n-3 10.1 f0.2221611-3 8.5 f 0.5z 20.2

1 o f 0.32.3 f 0.69.5f2.11.4zt0.2

14.211.8+0.210.6*0.24.4 f 0.25.7 *0.48.6kO.4

41.1O.S+O.l0.6+0.20.7 f 0.040.2 f 0.0411.650.38.7 f 0.3

22.6Total 78.2 77.9

2.2* 1.01.9f0.2

12.3 f 1.11.9f0.3

18.31.9 f 0.7

15.6f0.39.2 f 0.45.4 + 0.84.4* 1.1

42.51.3jzO.20.8 f 0.20.4 f 0.20.3f0.113.1f0.9

11.6f 1.021.588.3

1.1 f0.4b2.3 f 0.9b

12.3k2.41.9fO.lb

17.69.5 + 0.7

13.9* l.lb7.2 f 0.65.3 f 0.55.3f0.2

41.20.7*0.10.6 f 0.040.3 f 0.010.2 f 0.0312.3f0.2

10.3 * 0.5b24.483.2

0.7 f 0.31.7*0.95.8 rt2.71.1*0.29.37.1 f l.Sb7.7 f 1.6b4.1 * 1.33.7f0.Sb5.7 f 0.7b

28.30.7 f 0.20.6 f 0.21.0*0.1s0.1 *o.o3b21.61t6.6b

20.7 f 6.2b45.082.6

1.1 fO.l1.4 f 0.2b6.3 f 0.3b0.9f0.1b9.75.6 f 0.6

10.2f 1.3b5.2f0.6b2.7 f 0.22.1 fO.lb

25.80.8fO.l0.5 f 0.020.3 f 0.030.2 f 0.0222.3 + 1.3

24.8 c 1.748.984.4

Results are expressed as means f standard deviations of triplicate sample determinations.16:ln-7+ 16:ln-9.Significantly different (P < 0.05) from the same SW lipid fraction.Very significantly different (P < 0.01) from the same SW lipid fraction.

Only low concentrations of free all-trans Ax were found in saponified samples by thereversed-phase HPLC method, particularly from the SWS treatment (Table 2). Saponifi-cation (Kimura et al., 1990) applied to the SW and SWS oil extracts produced similar


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356 A. Guillou et al. /Aquaculture 130 (1995) 351-360

cso Monoester DiesterFRACTION

Fig. 1. Mean percentage of n-3 fatty acids (% of the total fatty acids) determined in crude shrimp oil (CSO) andin esterified astaxanthin fractions (mono- and diester) obtained from shrimp waste (white columns) and shrimpwaste silage (black columns).quantities of Ax derivatives like astacene, the oxidized form of Ax, and some Ax isomers.A larger destruction of Ax from SWS during saponification seems to be the best explanationfor the difference (P < 0.05) in all-trans Ax concentrations observed between SW and SWSoil extracts (Table 2). Surprisingly, no other carotenoid pigment phoenicoxanthin, can-thaxanthin, echinenone and p-carotene) could be identified from SW or SWS by the HPLCmethod. Free all-trans Ax seemed to be more concentrated in condensed oil from SW (Table2). This was also observed for the relative abundance of free Ax in oil from SW (Table 3)but these differences were not significant (P> 0.05). In SW and SWS oil extracts, thepredominant forms of Ax were the diester ( = 76%)) monoester (l&20%) and free Ax(6-4%), respectively. These results are in accordance with those reported for the sameshrimp species (Renstrom et al., 1981; Torrissen et al., 1981) Moreover, there were nosignificant differences (P > 0.05) in the percentages of Ax forms obtained from the SWand SWS samples (Table 3). These results indicate that no transformation of the diesterfraction into monoester fraction took place in the SWS samples.Fatt y acids

In Table 4, statistical comparisons are made between lipid fractions (crude shrimp oil,Ax mono- and diester) of SW and SWS. The major saturated and PUFAs seem to be slightlymore esterified with Ax in the diester form whereas the monounsaturated fatty acids areequally represented in spite of great variations among some individual fatty acids ( 18: 1 and22: ln-9).

Although small differences existed between the fatty acid profiles of crude oil from SWand SWS, fatty acid profiles from the mono- and diester Ax fraction before and after thesilage treatment were significantly different (Table 4). A sharp decrease of the relativeamount of the saturated and monoenoic fatty acids esterified with Ax in the SWS sampleswas offset by an increase of two polyenoic fatty acids, the 205-3 (EPA) and the 22:6n-3(DHA). This increase induced a 2-fold rise in the relative proportion of n-3 fatty acids


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associated as mono- (22 to 44%) and diester (26 to 48%) to Ax in SWS compared to SW(Fig. 1) . The large quantity of EPA and DHA esterified to Ax observed in the SWS samplescan probably explain why the crude oil extracted from the SWS contained slightly more(P < 0.05) n-3 fatty acids than the crude oil from defrosted SW (Fig. 1 and Table 4).4. Discussion

Astaxanthin formsThe results presented in Table 1 indicate that the extraction method permitted the complete

extraction of the lipids from the SW but failed to extract a small part of red carotenoidpigment (probably Ax) firmly bound to the carapace of the shrimp. These pigments pro-duced the light orange colour of the SW after the solvent extraction. Fox (1973) reportedthat hot acetic acid decalcified the crab shell and made possible the extraction of all carot-enoid pigments with common organic solvents (acetone or methanol). Omara-Alwala etal. ( 1985) reported that the use of propionic acid enhanced the recovered Ax concentrationby 35% in vegetable oil from whole crawfish waste. In our experiment, the silage procedureled to an increase in Ax concentration of only 14.5% (Table 1). This may be explained bythe fact that acetone or PE more effectively extract carotenoid pigments than does vegetableoil. The large beneficial effect of acidification, observed when oil is used for lipid extraction,is weaker when organic solvents are utilized.

Schiedt ( 1987) emphasized that carotenoid pigments should be saponified in the absenceof oxygen, under anaerobic conditions or at least under a nitrogen atmosphere. This sapon-ification technique would probably reduce the oxidation of Ax observed in our saponifiedsamples (Table 2).

Torrissen et al. (1981) reported that a conversion of the Ax diester to correspondingmonoester forms took place, after 21 days, in the SWS stored at 4-5C. In our conditions,the same proportions of the three Ax forms in lipid fractions was observed for defrostedSW and SWS after 14 weeks of storage (Table 3). This clearly shows the absence of SWdecomposition and good preservation of Ax when our mixture of acids and antioxidantswas used.

Fatty acidsThe fatty acid profiles of crude oil extracted from defrosted SW and SWS were very

similar and comparable to those presented for the whole body of P. borealis (A&man andEaton, 1967) or for its processing waste (Shahidi et al., 1992). Nevertheless, our profile offatty acids esterified with Ax in SW appears to be different from the profile previouslyreported by Renstrom and Liaaen-Jensen ( 1981).

The large increase of the relative quantities of EPA and DHA in esterified Ax fractionsfrom the SWS is quite surprising. Our explanation of this observation is that the redcarotenoid pigment firmly bound to chitin in the shrimp carapace and only completelyextracted in SWS was in fact Ax, almost exclusively mono- and diesterified to EPA andDHA. This supposition is supported, at least in part, by a study made with a freshwatercopepod. Vincent and Ceccaldi ( 1988) have reported that the unsaturation level of PUFAsesterified to carotenoids increased with the increasing level of oxygenation in pigments. As


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358 A. Guillou et al. /Aquacuhre 130 (1995) 351-360

Ax is one of the most oxygenated carotenoids, it seems possible that a large proportion ofAx could be esterified with long-chain PUFAs.SWS as pi gment i ng i ngredi ent for salmoni d feedsSWS could be incorporated into moist (Torrissen et al., 1981; Tidemann et al., 1984;Ouellet et al., 1992) and dry feeds (personal work) to provide a natural source of dietaryAx to salmonids. As consumers are sensitive to food ingredients and additives, cultured fishwith a natural pigmented label should be a good marketing argument for salmonidproducers. Our SWS (35.8 mg/kg) added to 25-30% (wet weight) of the feed will give apigmented feed with a final Ax content of 10-l 1 mg/kg. More concentrated SWS could beobtained by dewatering SW before the acid preservation (Tidemann et al., 1984). Thisprocess would increase the total Ax concentration in the feeds to about 15-20 mg/kg. Theseconcentrations are 2- to 4-fold smaller than those of commercial finishing feeds containingsynthetic free Ax (40-60 mg Ax/kg of feed). To save on expensive pigmented finishingfeeds (Torrissen et al., 1989), economical pigmentation strategies could be elaborated fordifferent species of cultured samonids with diets containing low concentrations of SW Ax(5-20 mg/kg) but given to fish during longer periods of time (a few weeks to severalmonths). In fact, for rainbow trout Oncorhynchus mykiss) the retention coefficient of Axdecreased as the pigment concentration in the diet increased. The maximum retentioncoefficient was observed with diets containing 3.4 mg of SW Ax/kg (Torrissen, 1985) and25.0 mg of synthetic Ax/kg (Choubert and Storebakken, 1989). Smith et al. (1992)suggested that an economical pigmented diet for pan-size coho salmon (0. kisutch) wouldcontain 15 mg of synthetic Ax/kg and fish from 50 g should be fed throughout the productioncycle (28 weeks).For us, the major problem for the utilization of SWS in commercial pigmented feedscomes from the unknown variations of its Ax content over the fishing season of P. boreal i s(May to early November). In fact, great variations in lipid and fatty acid contents arecurrently reported for the same fish species (Stansby et al., 1990). Moreover, in wildcrustaceans, the metabolism of lipids and carotenoids follows a similar pattern (Vincentand Ceccaldi, 1988) and it will be influenced by many seasonal factors (Jeckel et al., 1991))where the most important are the water temperature, the sexual maturation and the moultingcycle (Goodwin, 1960; Vincent et al., 1988; Vincent, 1989). Investigations are needed tocharacterize these variations in Ax and lipid concentrations over the 6-month period of SWproduction. The results would permit one to define the best strategy to obtain a uniformSWS product acceptable for fish feed manufacturers.

In conclusion, the silage treatment with antioxidants, despite its low pH, has proved tobe very effective in protecting SW against degradation. All Ax forms and PUFAs are wellstabilized and any loss in these unstable compounds has been observed after 3 months ofsilage storage. This technique could therefore be used to economically preserve shrimpwaste during storage and transport before it is incorporated into fish feeds or before extrac-tion of its value-added products such as astaxanthin, lipids, proteins and chitinlchitosan.

AcknowledgementsThe autors thank Dr. G. Negre-Sardagues (Laboratoire deco-physiologie des invertebres,

USTL, Montpellier) for bibliographic help, and Mrs. D. Betube, Mrs. P. Saucy and Mr. L.


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Fournier for their valuable technical assistance. We also thank Hoffmann-La Roche (Basel,Switzerland) for providing us with authentic carotenoids. This work was financially sup-ported by Le Fonds de Developpement Acadtmique du RCseau de 1Universite du Quebec(FODAR) and by La Fondation de 1Universitt du Quebec a Rimouski Inc FUQAR) .The first author was supported by postdoctoral awards (NSERC and UQAR .ReferencesAckman, R.G. and Eaton, CA., 1967. Fatty acid composition of the decapod shrimp, Pandalus borealis, in relation

to that of the euphausid, Meganyctiphanes noruegica. J. Fish. Res. Board Can., 24: 467-471.AOAC, 1990a. Fatty acids in oils and fats: preparation of methyl esters (Method 969.33). In: K. Helrich (Editor),

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Meyers, S.P. and Thibodeaux, P., 1983. Crawfish wastes and extracted astaxanthin as pigmentation sources inaquatic diets. J. Aquaric. Aquat. Sci., 3: 63-70.

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