Effect of Spirulina platensis Meal as a Feed Supplement on Growth Performance and Pigmentation of Rainbow Trout (Oncorhynchus mykiss)

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1 World Journl of Fish nd Mrine Sienes 5 (2): , 203 ISSN IDOSI Pulitions, 203 DOI: /idosi.wjfms Effet of Spirulin pltensis Mel s Feed Supplement on Growth Performne nd Pigmenttion of Rinow Trout (Onorhynhus mykiss) Mhdi Teimouri, Adolsmd Kermt Amirkolie nd Sekineh Yegneh Deprtment of Fisheries, Fulty of Animl Siene nd Fisheries, Sri Agriulturl nd Nturl Resoures University, Km 9 Dry Boulvrd, Sri, Irn Astrt: This study evluted the effets of diets ontining 0, 2.5, 5, 7.5 nd 0% Spirulin pltensis nd 50 mg of syntheti stxnthin kg on skin nd fillet pigmenttion nd growth performne of rinow trout (Onorhynhus mykiss). A ompletely rndomized experimentl design ws developed with six tretments (three replites eh). Two hundred nd sixteen rinow trout with verge initil weight of 0±8 g were ssigned to eighteen experimentl tnks. The experiment lsted for ten weeks. Addition of S. pltensis did not influene growth relted prmeters (P>0.05). However, rotenoid onentrtions of skin nd fillet signifintly inresed with inresing the levels of the lg (P<0.05). Inlusion of 0% S. pltensis s nturl pigment soure resulted in the highest rotenoid deposition in oth tissues. The highest vlues of * (redness) nd * (yellowness) were oserved in fish fillet fed with0% S. pltensis. In the skin, however, the highest vlue ws found for fish fed syntheti stxnthin. In ddition, feeding on ontrol diet signifintly inresed L* (luminosity), C* (hrom) nd H (hue) in oth skin nd fillet ompred to feeding with other diets. The present results demonstrted tht S. pltensis n e introdued s n lterntive nturl rotenoid soure insted of syntheti stxnthin in rinow trout diets. Inlusion of 5% S. pltensis ws found to e suitle dietry level to ensure pigmenttion s well s no negtive effets on fish growth. Key words: Spirulin pltensis Pigmenttion Growth Performne Rinow Trout INTRODUCTION hromtophores, whih re lrge, str-shped, pigmentontining ells loted in the skin. Fish hve multiple There re four min pigment groups tht give olor to hromtophores: melnophores, xnthophores, skin nd tissues of nimls nd plnts, nmely: melnines, erythrophores, iridophores, leuophores nd purines, pteridiums nd rotenoids. Crotenoids re ynophores. Colors in the yellow-to-red rnge re responsile for red, ornge nd yellow olors of fish nd produed y xnthophores nd erythrophores [5]. rustens []. A distinguished feture of slmonids is Crotenoids suh s stxnthin nd nthxnthin their ility to deposit ingested rotenoids in their re ommonly used in quulture s pigmenttion musle. Nowdys musle pigmenttion imprted y soures [6]. However, reent efforts hve foused on these lipophili ompounds hs eome n importnt nturl ompounds s lterntives to syntheti qulity riterion for the onsumers [2]. Slmonids like rotenoids euse of onerns out the use of other nimls nnot synthesize rotenoids de novo; syntheti dditives nd their high ost. Nturl soures therefore, they depend entirely on dietry supplements of rotenoids suh s Xnthophyllomyes dendrorhous to hieve their nturl pigmenttion [3]. [7], Hemtoous pluvilis [3] nd Cpsium nnuum Aout 90% of rotenoids found in tissues re [6] hve een tested on pigmenttion of slmonids; loted in flesh in their free form, ut lrge mounts re however, low digestion of plnt mtters y fish my lso found in the skin nd ovries in mturing fish [4]. redue the vilility of pigments y digestive trt of Skin olor is primrily dependent on the presene of fish [3]. Corresponding Author: Mhdi Teimouri, Deprtment of Fisheries, Fulty of Animl Siene nd Fisheries, Sri Agriulturl nd Nturl Resoures University, Km 9 Dry Boulvrd, P.O. Box: 578, Sri, Irn. Tel: , Fx:

2 World J. Fish & Mrine Si., 5 (2): , 203 Unlike these orgnisms, Spirulin pltensis does not hve ellulose ell wll. Its ells hve muopolymer murein tht is esily digested y the digestive enzymes sereted y fish [8]. S. pltensis is photosyntheti, filmentous, lue-green mirolge nd is generlly regrded s rih soure of vitmins, essentil mino ids, minerls, essentil ftty ids ( -linoleni id) nd ntioxidnt pigments suh s rotenoids nd phyoynin [9]. S. pltensis n enhne the nturl muous lyer of the skin resulting in shiny pperne of the fins nd skin [0]. As pigmenttion dditive, S. pltensis ws found to enhne the olor of red tilpi [], Mekong gint tfish [2], goldfish [0] nd prwn [3]. As feed ingredient, there hve een severl studies on lge mel s dietry protein soure for fish. It hs een onfirmed tht ddition of smll mounts of lge to fish feed n exert pronouned effets on growth, lipid metolism, ody omposition nd disese resistne [4]. Feeding S. pltensis tivted protein synthesis nd somti growth in red se rem [4], guppy [5], Afrin shrptooth tfish [6] nd Indin rps [7]. Hene, S. pltensis my hve potentil to e used s nturl feed supplement for inresing fish growth nd pigmenttion. Therefore, the min ojetive of the present study is to investigte the effets of S. pltensis on growth prmeters nd lso its potentil s n lterntive nturl rotenoid soure to syntheti stxnthin in rinow trout diets. MATERIALS AND METHODS Experimentl Diets: Five diets were formulted using the mirolge S. pltensis (Sinmirolge Co., Qeshm, Irn). Sine the proximte omposition of S. pltensis nd fish mel ws nerly similr, the lg ws sustituted for 0, 2.5, 5, 7.5 nd 0% of the dietry fishmel. Zero perentge ws designted s ontrol diet. The sixth experimentl diet ws lso dded for ompring hemil nd nturl pigments. In this diet, Luntin Pink (50 mg kg ; BASF, Ludwigshfen, Germny) ws used s soure of syntheti stxnthin. The formultion nd proximte omposition of ontrol diet, S. pltensis nd fish mel re given in Tles nd 2, respetively. Dietry feed ingredients were ground using lortory grinder nd then lended into homogenous doughy mtter y dding wter, whih pelleted y pressing through 4 mm die in grinding mhine. The pellets were then stored in plsti ontiners t -30 C until use. Tle : Feed ingredients nd nutrients omposition (% dry weight) of the experimentl diet 37. Ingredients 38. % 39. Soyen mel fish mel Whet gluten 4 Whet flour 5 Met mel 8 Fish oil 6 Soyen oil 6 Minerl premix 0.5 Vitmin premix 0.5 Binder 2 Proximte omposition Dry mtter 90 Crude protein 42 Crude lipid 7 Crude fier.3 Ash 0 Energy (kl g ) 3.8 Minerl premix onsisted of (mg kg premix): 2600 mg Mn, 600 mg Cu, 6000 mg Fe, 4600 mg Zn, 50 mg Se, 00 mg Iu, 50 mg Co, mg holin hloride, up to kg rrier. Vitmin premix onsisted of (mg kg premix): IU Vitmin A, IU Vitmin D3, 3000 IU Vitmin E, 200 mg K3, 5400 mg C, 200 mg H2, 200 mg B, 3360 mg B2, 7200 mg B3, 9000 mg B5, 2400 mg B6, 600 mg B9, 4 mg B2. Eh vlue is the men of three su-smples Tle 2: Proximte omposition of spirulin nd fish mel used in the experiment (%) Ingredients Proximte omposition (%) Spirulin Fish mel Dry mtter Crude protein Crude lipid All fish were fed the ontrol diet during the first 7 dys fter stoking to dpt them to feeding nd hndling prties. After tht, the fish were fed with the experimentl diets. Fish Rering nd Smpling: Fish (n= 26; 0±8 g) were rndomly divided into eighteen 300L fierglss tnks in triplites (2 fish per replition). The whole wter of the tnks ws exhnged with well wter every dy. Wter qulity prmeters were heked three times per week fter the first feeding. Those prmeters were kept within optiml rng for rinow trout; temperture3±2 C, slinity 0.6±0. ppt, ph 7.6±0.2 nd dissolved oxygen (DO) 8.6±mg L. All tnks were mintined under onstnt photoperiod (2 h drk: 2 h light) reted y fluoresent lmps. Fish were fed y hnd, twie per dy t rte of 2% of ody weight during the experiment. 95

3 World J. Fish & Mrine Si., 5 (2): , 203 The experiment lsted for ten weeks. On the lst dy ws determined spetrophotometrilly in etone using of the experiment, ll fish were weighed individully. extintion oeffiients (E%, m) 2500 for rotenoids Afterwrd, three fish were rndomly seleted from eh t 450 nm. Totl determined rotenoid ontent of tnk nd srified using 300 mg L love essene the S. pltensis mel ws.26 mg g. solution. The left fillet ws seleted for olor nlysis. Sttistil Anlysis: All dt were expressed s the Photogrph Anlysis: Photogrphs were tken ording men ± SD. All dt were verified for normlity fter to Tlusty nd Hylnd [8]. Nikon D80 digitl SLR mer trnsformtion (ASIN). One-wy ANOVA ws used to ws used for this purpose. The mer ws mounted on determine the effets of S. pltensis on growth tripod etween the two light sides. The mer ws set performne nd pigmenttion using SPSS (version 7). up t 25 m ove the speimens nd ould pture the Dunn s multiple rnge test ws used to ompre whole fish imge. Photogrphs of skin (whole fish) nd differenes etween the mens t 5% proility. Liner fillet were tken under these onditions: shutter speeds regression nlyses were lso used to relte rotenoid were 0, perture ws F6 nd zoom ws 35. The imges onentrtions nd olor prmeters. were nlyzed with Adoe Photoshop CS4 softwre (version ). Pitures were opened in RGB mode. RESULTS Mesurements were proessed t three lotions long the fillet nd skin ove the lterl line; lose to the hed, S. pltensis supplemented diets did not hnge midwy etween the hed nd the til nd lose to the til. growth relted prmeters in rinow trout, lthough In eh position, five repetitions were reorded nd the lrger weight gin nd SGR were oserved in rinow verge vlue ws used in this study. The tristimulus trout fed diet ontining 7.5 nd 0% S. pltensis L*** mesurement mode ws used s it reltes to the ompred to the other tretments (Tle 3). FCR ws not humn eye response to olor. The L* vrile represents lso influened y S. pltensis inlusion (p>0.05). lightness (L* = 0 for lk, L* = 00 for white), * sle Color dt showed tht the fish fed diets ontining represents the red/green, +* intensity in red nd -* nturl nd/or syntheti pigments turned to pinkish t the intensity in green. The * sle represents the end of the experiment (Tle 4). In ontrst, ll fish fillet in yellow/lue, +* intensity in yellow nd -* intensity in the ontrol group were poorly pigmented. * nd * lue. The hrom is n expression of the intensity nd inresed with inresing the levels of S. pltensis in the lrity of the olor nd the hue is n ngulr mesurement diets. The fish fed 0% S. pltensis displyed more where 0 indites red hue nd 90 denotes yellow reddish hue thn those of ontrol nd 2.5% S. pltensis. hue. Feeding on ontrol diet inresed signifintly L*, C* nd H ompred to feeding on the other diets (p < 0.05). Crotenoid Anlysis: The rotenoid ontent ws The highest levels of fillet pigmenttion nd extrted ording to the method of Torrissen nd rotenoid deposition were found in0% S. pltensis Nevdl [9], with some modifition. Smples of g skin (Fig. ). However, there were no differenes in rotenoid were olleted from oth sides etween the dominl onentrtion of the trout's fillet fed 2.5, 5% S. pltensis nd dorsl regions of the fish, eing reful to remove nd stxnthin diets. Control diet hd the lowest dhering dipose tissue. The smple ws then trnsferred rotenoid onentrtion. to 0 ml pre-weighed glss tues nd ground in 0 ml Regression nlysis indited tht olor prmeters etone (98%, Merk, Germny) ontining nhydrous re signifintly orrelted to rotenoid onentrtions sodium sulphte with homogenizer (Ultr-turrx IKA (Fig. 2). T8 si). The smples were stored for one dy t 4 C As shown in Tle 5, skin luminosity (L*) ws not nd then extrted with etone two or three times until ffeted y the tretments. * nd * inresed no more olor ould e otined. The solutions were signifintly with inresing S. pltensis inlusion, entrifuged t 3500 rpm for 0 min nd then sorptions ut fish fed stxnthin presented the lrgest estimtes of were mesured y spetrophotometer (Unio S-250UV). * nd * (P<0.05). In ddition, C* nd H showed n A similr method ws used for totl rotenoid indiret reltion with the inresing levels of S. pltensis. nlysis of fillet nd S. pltensis. Approximtely 25 g of Although oth S. pltensis nd syntheti stxnthin fish fillet ws mined y food proessor for 5-0 s nd signifintly elevted the rotenoid onentrtion then 5 g su-smples nlyzed for rotenoid ontent. (Fig. 3), mximum rotenoid skin ontent ws oserved Totl rotenoid onentrtion of skin, musle nd lge with 0% S. pltensis. 96

4 World J. Fish & Mrine Si., 5 (2): , 203 Fig. : Fillet rotenoid onentrtion (mg kg ) in rinow trout feeding on different levels of S. pltensis nd syntheti stxnthin over 0 weeks experimentl period All vlues re mens of three replites (tnks)/tretment ± stndrd devition Tle 3: Growth performne in rinow trout feeding on different levels of S. pltensis nd syntheti stxnthin over 0 weeks experimentl period Diets Growth prmeters Control AST SP 2.5 SP 5 Sp 7.5 SP 0 Initil weight (g) 0.9 ± ± ± ± ± ± 0.9 Finl weight (g) ± ± ± ± ± ± 3.5 Weight gin (%) 20.7 ± ± 23.4 ± ± ± ±. SGR (%/dy).3 ± ± ± ± ± ± 0.08 FCR.3 ± ± ± ± ± ± 0. Vlues re mens of triplite groups ± SD. Mens with the different supersript letters re signifintly different (P<0.05) Tle 4: Color prmeters of fillet in rinow trout feeding on different levels of S. pltensis nd syntheti stxnthin over 0 weeks experimentl period Diets Color prmeters Control AST SP 2.5 SP 5 Sp 7.5 SP 0 Luminosity (L*) 33. ± ±.3 3. ± 29.6 ±.7 d 27.6 ± 0.7 d 25.5 ± Redness (*) 4.3 ±.2 ± ± ±.5. ± ±.6 Yellowness (*) 3. ±.2 7 ±.5 4 ± 9. ± ±.8 4. ±.8 Chrom (C*) 59 ±.5 5. ± ± ± ±.2 46 ±.3 Hue (H ) 25.5 ±.5 5. ± ± ± ± ± 2.2 Vlues re mens of triplite groups ± SD. Mens with the different supersript letters re signifintly different (P<0.05) Tle 5: Color prmeters of skin in rinow trout feeding on different levels of S. pltensis nd syntheti stxnthin over 0 weeks experimentl period Diets Color prmeters Control AST SP 2.5 SP 5 Sp 7.5 SP 0 Luminosity (L*) 38.5 ± ± ± ± ± ± 4.8 Redness (*) d 3.5 ±. 5.5 ± ± 6.3 ± ± ±.5 Yellowness (*) 8.2 ± ± ± ±. 3.6 ± ± 0.8 Chrom (C*) 53.8 ±.9 d 43. ± ± ± ± ± 2.5 Hue (H ) 27.5 ± ±. 23 ± ± ± ±3.2 Vlues re mens of triplite groups ± SD. Mens with the different supersript letters re signifintly different (P<0.05) 97

5 World J. Fish & Mrine Si., 5 (2): , 203 Fig. 2: A omprison etween fillet rotenoid onentrtion nd () L*, () *, () *, (d) C* nd (e) H in rinow trout feeding on different levels of S. pltensis over 0 weeks experimentl period Fig. 3: Skin rotenoid onentrtion (mg kg ) in rinow trout feeding on different levels of S. pltensis nd syntheti stxnthin over 0 weeks experimentl period All vlues re mens of three replites (tnks)/tretment ± stndrd devition 98

6 World J. Fish & Mrine Si., 5 (2): , 203 Fig. 4: A omprison etween fillet rotenoid onentrtion nd () L*, () *, () *, (d) C* nd (e) H in rinow trout feeding on different levels of S. pltensis over 0 weeks experimentl period Exept L*, other olor prmeters were orrelted to unlike plnt ingredients, inlusion of S. pltensis s feed skin rotenoid onentrtion (Fig. 4), showing tht the dditive my improve feed effiieny y inresing gut ddition of S. pltensis hd n impt on skin olor. teril oloniztion. Although the tion mehnism of S. pltensis is not lerly demonstrted, Jmes et l. [2] DISCUSSION suggested tht S. pltensis improves the intestinl flor in fish rendering rek down of indigestile feed The results showed tht replement of fishmel with omponents to extrt more nutrients from the feed; this S. pltensis up to 0% did not hve negtive impts on lso stimultes the prodution of enzymes tht trnsport growth performne in rinow trout. This finding is fts within the fish for metolism insted of storge. similr to tht reported y Nndeesh et l. [7] who The urrent study showed tht feeding dietry found tht replement of fishmel with S. pltensis up S. pltensis inresed pigmenttion in rinow trout. to 00% did not deline growth rte in Indin rps Similr results were otined y Mori et l. [22], (Ctl tl nd Leo rohit). Similrly, Olver-Novo Okd et l. [23] nd Promy nd Chitmnt [6], who et l. [20] nd Derneksi et l. [5] oserved tht oserved tht S. pltensis ddition to the diets improved repling fishmel with S. pltensis up to 40% did not pigmenttion in Afrin shrptooth tfish, striped jk hnge growth rte in tilpi nd guppy. A tendeny nd sweet smelt. Moreover, Tongsiri et l. [2] oserved towrd etter growth performne t 7.5 nd 0% tht feeding S. pltensis improved texture together with S. pltensis oserved in the urrent study suggests tht, pigment enhnement in Mekong gint tfish. 99

7 World J. Fish & Mrine Si., 5 (2): , 203 It hs een found tht stxnthin to e the most hve een used y hrteristis of skin ells. effetive pigment to enhne pigmenttion in Skin xnthophores tht ontin rotenoid droplets slmonids [24]. Although the mjor rotenoid soures of [32] my e esier sturted with stxnthin. This se S. pltensis re -rotene nd zexnthin [3], our results remins to e further investigted. showed tht the ddition of S. pltensis to the rinow The results lso showed tht olortion nd trout diet led to pigment deposition in fillet. There is some onentrtion of rotenoids in rinow trout re linerly evidene showing tht zexnthin is lso deposited s relted. Severl mthemtil models tht desrie the pigment in tissue. Shiedt et l. [25] oserved tht reltionship etween instrumentlly ssessed olortion stxnthin deposition effiieny is lrger thn other nd rotenoid onentrtion showed tht instrumentl rotenoids followed y doniruin, nthxnthin, olor nlysis under stndrd onditions n e used to zexnthin, lutein nd finlly -rotene. Ktsuym et l. predit rotenoid levels urtely [7]. A hnge in fish [26] found tht dietry stxnthin ws mostly sored, olor prmeters nd lso liner orreltions oserved in umulted nd prtilly metolized to zexnthin in the urrent study is in greement with Wthne et l. [33], rinow trout. It, therefore, ppers tht pigmenttion in Storekken et l. [7] nd Mor et l. [6]. The inrement fish musle fed S. pltensis in the urrent study is lso in the verge vlues of * nd * nd derement of H used y deposition of zexnthin s mjor rotenoids with inresing dietry rotenoid onentrtion is in in S. pltensis. greement with Mor et l. [6] nd Chouert et l. [34, 35]. Fillet pigmenttion t 7.5 nd 0% S. pltensis ws However, S. pltensis ddition deresed C* vlue in signifintly higher thn the other groups. This result ws ontrst to Mor et l. [6] nd Chouert et l. [34, 35]. expeted due to n inrese in diet rotenoid The derese in L* vlues my e relted to the fillet ft onentrtion. Regrding the two rotenoid soures, ontent. Nikell nd Bromge [36] reported tht L* ws there were no differenes in the musle pigmenttion signifintly orrelted to flesh lipid ontent, thus etween fish fed 5% S. pltensis nd those fed syntheti hnges in ft ontent of fillet my hve used this stxnthin hving lmost similr pigment doses. derement in L*. Wtne nd Vssllo-Agius [27] lso Despite dietry stxnthin is more effetive thn reported tht the Spirulin supplemented diets improved zexnthin in terms of deposition, feeding on S. pltensis the flesh qulity of ultured striped jk minly y supplemented diets my hve enhned rotenoid depressing the umultion of lipids. iovilility. Wheres the effiieny of utiliztion of dietry stxnthin for flesh pigmenttion of Atlnti CONCLUSION slmon nd rinow trout rrely exeeds 0-5% [27] esy rekge of S. pltensis ell wll my explin the The results of present study demonstrte the similr levels of rotenoid deposition in the fish fillet potentil of S. pltensis s feed dditive to indue ompred to the stxnthin tretment. S. pltensis hs rinow trout pigmenttion, whih ould ffet the thin ell wll omprised of 80% petin nd 20% ellulose mrket qulity nd eptility of the fish. S. pltensis [28], thus its rotenoid ontent n e esily ssimilted n lso e supplemented in diet s n effetive nturl y digestive trt. Pigmenttion of rinow trout fed rotenoid soure insted of syntheti stxnthin for disrupted ells (ell wll rked) of H. pluvilis ws fillet pigmenttion of rinow trout. However, etter thn rinow trout fed diets ontining intt ells pigmenttion is not equl in oth skin nd fillet. from H. pluvilis [29]. Furthermore, sine rotenoids re Moreover, this study showed tht S. pltensis n e ft-solule pigments, highly unsturted ftty id used s fishmel replement in rinow trout diets due ontent of S. pltensis my inrese the pigments to its high protein ontent nd no negtive impts on sorption [30]. In ddition, the S. pltensis rotenoid fish performne. might e more esily dissolved in the dietry lipids, wheres ommeril produts, t lest prtly, onsist of REFERENCES nnoprtiles nd ggregtes [3], whih need to e dissolved prior to sorption.. Kop, A. nd Y. Durmz, The effet of syntheti In ontrst to fillet, skin pigmenttion ws higher for nd nturl pigments on olor of Cihlids stxnthin diet even though t highest rotenoid (Cihlsom severum, Hekel 840). Aquult. Int., onentrtion (0% S. pltensis). This ondition my 6:

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