Effects of different algae in diet on growth and interleukin (IL)-10 production of juvenile sea cucumber Apostichopus japonicus

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1 Anisuzzmn et l. Fisheries nd Aquti Sienes (217) 2:24 DOI /s RESEARCH ARTICLE Effets of different lge in diet on growth nd interleukin (IL)-1 prodution of juvenile se uumer Apostihopus jponius Open Aess Md Anisuzzmn 1, Jeong U-Cheol 1, Jin Feng 1, Choi Jong-Kuk 1, Kery Kmrunnhr 1, Lee D-In 2, Yu Hk Sun 2 nd Kng Seok-Joong 1* Astrt The experiment ws onduted to investigte the effets of different lge in diet on growth, survivl, nd interleukin-1 produtions of se uumer. At first, 9-week feeding tril ws onduted to evlute the growth performne nd survivl of the se uumer fed one of the six experimentl diets ontining ST (Srgssum thunergii), UL (Ulv ltu), UP (Undri pinntifid), LJ (Lminri jponi), SS (Shizohytrium sp.), nd NO (Nnnohloropsis oult) in reirulting quulture system. The result showed tht survivl ws not signifintly different mong the dietry tretments, nd the speifi growth rte (SGR) of se uumer fed the UL diet (1.58% d 1 ) ws signifintly higher thn tht of se uumer fed the other diets (P <.5), exept for the LJ nd NO diets. Seondly, interleukin (IL)-1 gene expression ws determined where mie splenoytes were stimulted with 1 μgml 1 of se uumer extrts for 2 h. The result showed tht IL-1 gene expression levels were signifintly inresed in UL, LJ, nd NO diets fed se uumer extrts ompred to other experimentl diets. The results suggest tht dietry inlusion with Ulv ltu, Lminri jponi, ndnnnohloropsis oult lge my improve the growth of juvenile se uumer nd ould upregulte IL-1 gene expression in mie splenoytes. Suh detiled informtion ould e helpful in further development of more pproprite diets for se uumer ulture. Keywords: Se uumer (Apostihopus jponius), Alge, Growth, Interleukin (IL)-1 Bkground The se uumer, Apostihopus jponius, hs eome n importnt mriulture speies in Russi, Chin, Jpn, nd South Kore euse of its reltively high eonomi vlue (Slon 1984). Mrket demnd for this speies inresed euse of its phrodisi nd urtive properties (Lio 1997). However, the prodution of se uumers otined from the nturl environment hs delined due to overexploittion nd pollution (Connd 24). Depletion of wild prodution together with high ommeril vlue hs enourged the people to develop quulture methods for holothurins, espeilly A. jponius (Connd 24; Yun et l. 26). * Correspondene: sjkng@gnu..kr 1 Deprtment of Sefood nd Aquulture Siene, Gyeongsng Ntionl University, Tongyeong 5364, Repuli of Kore Full list of uthor informtion is ville t the end of the rtile Suessful ulture of juvenile se uumers requires proper knowledge out feed intke ehvior nd dietry requirements (Slter et l. 29). However, little is known regrding whih rtifiil diets re ple of induing rpid growth nd helthy onditions of ommerilly importnt se uumers (Slter et l. 29; Yun et l. 26; Zhou et l. 26). Se uumers re deposit feeders tht ingest sediment ontining orgni mtter, inluding teri, protozo, ditoms, nd detritus of plnts or nimls (Yingst 1976; Morirty 1982; Zhng et l. 1995; Feng et l. 216, 216). A. jponius preferentilly inhits the se ottom in flourishing lrge lge, rih detritus of whih provide se uumer with its min orgni nutrient (Li et l. 1994; Zhng et l. 1995). Trditionlly, se uumers re ultured in erthen ponds without rtifiil feed. But reently, frmers hve strted to feed the se The Author(s). 217 Open Aess This rtile is distriuted under the terms of the Cretive Commons Attriution 4. Interntionl Liense ( whih permits unrestrited use, distriution, nd reprodution in ny medium, provided you give pproprite redit to the originl uthor(s) nd the soure, provide link to the Cretive Commons liense, nd indite if hnges were mde. The Cretive Commons Puli Domin Dedition wiver ( pplies to the dt mde ville in this rtile, unless otherwise stted.

2 Anisuzzmn et l. Fisheries nd Aquti Sienes (217) 2:24 Pge 2 of 8 uumers with formulted diets to inrese prodution (Shi et l. 213). Formulted diets for se uumers re ommonly mde of mrolgl powder nd se mud. Among mrolge, the rown lgl Srgssum thunergii is widely distriuted over shllow ostl res in Kore, Jpn, nd Chin nd ommonly used s feed ingredient in se uumer ulture (Sui 1989; Bttglene et l. 1999). However, it is diffiult to stisfy demnd for se uumer ulture euse this lgl speies is not produed ommerilly nd its use s feed ingredients is lso expensive (Lon nd Hrrison 1994). In ddition, more nd more S. thunergii hve een hrvested in reent yers with the rpid expnsion of se uumer frming sle, whih results in severe dmge to S. thunergii resoure (Yun 25; Wng et l. 26). Menwhile, y feeding with ommeril feed whih mostly used S. thunergii, se uumer hve high level of n-6 ftty ids nd low n-3 ftty ids nd the lne of the n-3/n-6 rtio is not good (Feng et l. 216, 216). But n-3 ftty ids nd good lne of the n-3/n-6 rtio is very importnt to protet from llergi nd inflmmtory diseses like sthm. So, reduing the S. thunergii ontent of se uumer feed will e one strtegy to inrese the sustinility of the se uumer ulture. Therefore, it is ritil to find good sustitutes for S. thunergii to relieve the pressure on nturl S. thunergii resoure nd produe good qulity se uumer. Severl reserhers reported tht juvenile se uumers fed ommerilly ville dried powdered mrolge (Ulv ltu, Lminri jponi, Srgssum thunergii, Srgssum polyystum) nd se mud exhiited signifint growth (Bttglene et l. 1999; Liu et l. 21; Zhu et l. 27). In our study, we used Ulv ltu, Undri pinntifid, Lminri jponi, Nnnohloropsis oult, nd Shizohytrium sp. s prtil lterntive soure of Srgssum thunergii to produe signifint growth nd good qulity se uumer. Ulv ltu, Undri pinntifid, nd Lminri jponi re populr nd heper lge in Kore nd widely used in the ulture of se urhins nd lone (Agtsum 2, Qi et l. 21). Nnnohloropsis oult nd Shizohytrium sp. re onsidered promising lge for quulture nd offer high levels of polyunsturted ftty ids (PUFAs), espeilly eiospentenoi id (EPA, 2:5n-3) nd dooshexenoi id (DHA, 22:6n-3) respetively (Kndilin et l. 213 Yue et l. 24). Se uumers hve mny therpeuti effets ginst vrious diseses (Bordr et l. 211; Guo et l. 215). Moreover, se uumer extrts hve potent iologil effets nd hve ntivirl, ntiner, ntiteril, ntioxidnt, nd nti-inflmmtion effets (Esmt et l. 213; Frshdpour et l. 214; Kini et l. 214; Wijesinghe et l. 213). In Chin nd Mlysi, se uumers hve een trditionlly used for the remedy of different inflmmtory diseses like sthm. Asthm is hroni inflmmtory disese nd mjor puli helth prolem. Interleukin (IL)-1 is potent nti-inflmmtory ytokine tht downregultes the synthesis of Th1 (T helper 1)- nd Th2 (T helper 2)-ssoited ytokines, hemokines, nd inflmmtory enzymes. It plys vitl role for the mitigtion of llergi responses. But till now, there re no reports demonstrting the effet of different lge in se uumer on IL-1 prodution. In this study, the effets of different lge in diet on growth, survivl, nd nti-inflmmtory ytokine (IL-1) prodution of the juvenile se uumer were exmined. Methods Experimentl diets Six experimentl diets designed s Srgssum thunergii (ST), Ulv ltu (UL), Undri pinntifid (UP), Lminri jponi (LJ), Shizohytrium sp. (SS), nd Nnnohloropsis oult (NO) were prepred. Ingredients nd proximte ompositions of experimentl diets re presented in Tle 1. Most se uumers re deposit feeders tht ingest sediment with orgni mtter. Severl studies showed tht juvenile se uumers fed different lge nd se mud exhiited signifint growth (Bttglene et l. 1999; Liu et l. 29; Hi-Bo et l ST diet ws used s the ontrol diet where 15% Srgssum thunergii nd 15% whet flour were used. For diets UL, UP, LJ, SS, nd NO, whet flour ws repled y 15% UL, UP, LJ, SS, nd NO respetively. All ingredients were ground into fine powder through 2-μm mesh, thoroughly mixed, ndstoredt 2 C. Experimentl niml nd feeding tril The experiment ws rried out for 9 weeks in the lortory of Mrine Biology nd Aquulture, Gyeongsng Ntionl University, Repuli of Kore. Se uumers used in this experiment were olleted from the Goseong Se uumer frm. Prior to the experiment, se uumers were trnsferred to the lortory in fierglss quri nd limted for 2 weeks t 18 C. After 2 dys strvtion, 24 se uumers with initil wet ody weights of 2.98 ±.6 g (men ± SE) were rndomly seleted from limtized se uumers nd pled in equl numer into 24 fierglss quri ( m 3 ) to form six groups in tetrplite. The six groups were fed with different experimentl diets suh s ST, UL, UP, LJ, SS, nd NO respetively. A omplete rndomized lok design ws used to rrnge the 24 quri of six tretment groups.

3 Anisuzzmn et l. Fisheries nd Aquti Sienes (217) 2:24 Pge 3 of 8 Tle 1 Ingredients nd omposition of experimentl diets for Apostihopus jponius (% dry mtter sis) Ingredients ST (ontrol) UL UP LJ SS NO Ulv ltu powder 15 Undri pinntifid powder 15 Lminri jponi powder 15 Shizohytrium sp. powder 15 Nnnohloropsis oult powder 15 Whet flour 15 Seweed powder Soyen mel Shellfish powder Shell powder Clium phosphte Yest protein Soyen leithin Minerl premix Vitmin premix Se mud Proximte omposition (%) Crude protein Crude lipid Ash Minerl premix (g kg 1 premix): MgSO 4 7H 2 O, 8.; NH 2 PO 4 2H 2 O, 2.; KH 2 PO 4, 13.; Ferri itrte, 4.; ZnSO 4 7H 2 O, 1; C-ltte, 25.5; CuCl,.2; AlCl 3 6H 2 O,.15; KIO 3,.15; N 2 Se 2 O 3,.1; MnSO 4 H 2 O, 2.; CoCl 2 6H 2 O, 1. Vitmin premix (g kg 1 premix): sori id, 92.7; α-toopheryl ette, 14.5; thimine hydrohloride, 7; rioflvin, 7.; pyridoxine hydrohloride, 1.4; niin, 27.8; C-D-pntothente, 9.7; myo-inositol, 139.1; D-iotin,.5; foli id,.5; p-mino enzoi id, 13.9; mendione, 4.2; retinyl ette,.65; holeliferol,.8; ynoolmin,.4 During the experiment, ertion ws provided ontinuously nd to ensure wter qulity two thirds volume of the wter in eh qurium ws exhnged every dy. Sewter temperture ws ontrolled t 18 ± 1. C. Dissolved oxygen ws mintined ove mg l 1, nd the levels of mmoni in the wter of the quri were less thn.25 mg l 1. Other onditions were slinity 32 ± 1 ppt, ph , nd photoperiod 24-h drk. Proedure nd smple olletion Twenty-four se uumers were olleted s n initil smple efore strting the experiment. During the experiment, se uumers were fed one per dy (t out 17 hours). Uneten feed were olleted y siphon fter 24 h nd then dried t 65 C to onstnt weight. Se uumer fees were lso olleted y siphon one per dy (16 hours). The fees were dried t 65 C to onstnt weight, nd those from eh qurium were pooled for further nlysis. At the end of the 9- week experiment, ll the experimentl se uumers were deprived of food to ler their guts for 2 dys, weighed, nd then dried t 65 C until onstnt weight ws hieved. Dt lultion Survivl rte (SR), speifi growth rte (SGR), ingestion rte (IR), fees prodution rte (FPR), nd food onversion effiieny (FCE) were lulted s follows: SR ð% Þ ¼ 1 ðn 2 =N 1 Þ SGR %d 1 ¼ 1 ð lnw 2 lnw 1 Þ=T IR g g 1 d 1 ¼ I= ½ T ð W2 þ W 1 Þ=2 FPR g g 1 d 1 ¼ F= ½ T ð W2 þ W 1 Þ=2 FCE ð% Þ ¼ 1 ðw 2 W 1 Þ=I where N 1 is the numer of individuls live t strt of the experiment nd N 2 is the numer of individuls live t end of the experiment; W 1 nd W 2 re initil nd finl omined dry weights, respetively, of ll 1 se uumers in eh qurium; T is the experimentl period; I is the dry weight of the totl feed ingested; nd F is the dry weight of fees. Preprtion of se uumer extrt At first, our experimentl se uumers were lened nd the viserl orgns removed. After tht, the se

4 Anisuzzmn et l. Fisheries nd Aquti Sienes (217) 2:24 Pge 4 of 8 uumers were ut into smll piees nd homogenized. One hundred fifty grms of smples were oiled in 3 ml distilled wter for 2 min. After removing solid mterils from the wter, the oiled wter ws vporized using mirowve until the mixture ws redued y 5%. After entrifugtion of the extrts t 5 g for 1 min, fivefold volume of 1% ethyl lohol ws dded to the superntnt nd inuted t 2 C for 24 h. After tht, the superntnt ws disrded. The extrt pellet ws wshed with 7% ethyl lohol nd entrifuged under the sme onditions. The superntnt ws disrded, nd the pellet ws evported under vuum. The finl extrts were prepred y re-suspending the pellet in 2 ml distilled wter (Lee et l. 216). IL-1 gene expression In order to nlyze the IL-1 gene expression, mie splenoytes were stimulted with 1 μg ml 1 of eh experimentl diet-fed se uumer extrt for 2 h. The totl RNAs were isolted y Qizol regent (Qigen Siene, USA) ording to the mnufturer s protools. Two mirogrms of totl RNAs were trnsried using M-MLV reverse trnsriptse (Promeg, USA), ording to the mnufturer s protools. IL-1 mrna expression levels were synthesized y rel-time PCR using the icylertm (Bio-Rd Lortories, Herules, CA, USA). GAPDH ws used for the referene gene. IL-1 nd GAPDH primer sequene re previously desried (Lee et l. 216). Sttistil nlysis Sttistil nlysis ws performed y the softwre SPSS 18. with possile differenes mong diet tretments eing tested y using one-wy ANOVA. Tukey multiple omprison tests were used to nlyze the differenes mong tretments. Differenes were onsidered signifint t proility level of.5. Results Growth nd survivl The growth performne nd survivl of se uumer re shown in Tle 2. All se uumers were live t the end of the 9-week feeding tril. The growth performne of the se uumers differed signifintly mong tretments. Finl wet nd dry ody weights of se uumers showed the highest vlue for the UL diet group nd the lowest vlue for the ST diet group (P <.5). The highest SGR (1.58% d 1 ) ws oserved in se uumer fed the UL diet. SGR of se uumers fed the ST diet ws signifintly (P <.5) lower thn UL, LJ, nd NO diets, ut not signifintly (P >.5) different from tht fed the UP nd SS diets (Fig. 1). Ingestion rte nd fees prodution rte Ingestion rtes (Fig. 2) nd fees prodution rtes (Fig. 3) of the se uumers showed signifint differenes mong different diet tretments. Se uumers fed with diets LJ nd UL showed signifintly higher IR (.62 nd.59 g g 1 d 1 respetively) nd FPR (.53 nd.52 g g 1 d 1 respetively) thn those fed other diets (P <.5). Se uumers fed with diet ST showed the lowest IR (.32 g g 1 d 1 ) (P <.5) nd FPR (.26 g g 1 d 1 ) (P <.5) mong ll tretments. Food onversion effiieny Food onversion effiieny (%) ws signifintly different mong different diet tretments (Fig. 4). FCE of the se uumers fed with diet NO ws 3.74%, whih ws signifintly higher thn those fed with other diets (P <.5). Se uumers fed the diet UP showed the lowest FCE (2.21%). Anti-inflmmtory ytokine, IL-1 expression level In order to estlish proper lge for se uumer diet, we synthesize IL-1 gene expression levels. Splenoytes were stimulted with eh experimentl diet-fed se uumer extrt for 2 h. Result showed tht IL-1 gene expression levels were signifintly inresed in the UL, LJ, nd NO diets ompred to the other experimentl diets (Fig. 5). The highest IL-1 gene expression levels were found when the se uumers were fed the Ulv ltu lge diet. However, IL-1 gene expression levels were not inresed y ST, UP, nd SS diets nd hve no signifint differenes. These results suggest tht UL, LJ, nd NO lge ould upregulte IL-1 gene expression. Disussion In ll tretments, no se uumer died nd survivl rtes of se uumers were exellent (1%) nd were Tle 2 Initil nd finl wet weight (WW) nd dry weight (DW) of Apostihopus jponius fed different test diets (men ± SE) Experimentl diets Initil WW (g) Initil DW (g) Finl WW (g) Finl DW (g) Survivl (%) ST 3.4 ± ± UL 2.93 ± ± UP 2.94 ± ± LJ 3.3 ± ± SS 2.92 ± ± NO 3.2 ± ±

5 Anisuzzmn et l. Fisheries nd Aquti Sienes (217) 2:24 Pge 5 of SGR (% d -1 ) 1 FPR (gg -1 d -1 ) ST UL UP LJ SS NO Experimentl diets Fig. 1 Speifi growth rte of Apostihopus jponius fed different test diets. Different letters indite signifint differenes (P <.5) etween tretments within the sme group, nd rs represent stndrd errors ST UL UP LJ SS NO Experimentl diets Fig. 3 Fees prodution rte (FPR) of Apostihopus jponius fed different test diets. Different letters indite signifint differenes (P <.5) etween tretments within the sme group, nd rs represent stndrd errors higher thn the rtes reported in previous similr studies (Hi-Bo et l. 215; Slter nd Crton 27; Zhou et l. 26). The results showed tht se uumers might hve the ility to tolerte the different lge suh s UL, UP, LJ, NO, nd SS in diet. Systemti studies on the use of lge s n ingredient in ommeril feeds for se uumer ulture re very rre. Mny reserhers hve used different types of lge suh s Srgssum polyystum, Srgssum thunergii, Lminri jponi, Spirulin pltensis, Ulv ltu, Undri pinntifid, nd Pyropi spheroplsts to study se uumer nutrition requirements (Li et l. 29; Liu et l. 29; Seo nd Lee 211; Seo et l. 211; Slter et l. 29; Yun et l. 26, Shhuddin et l. 217). Most reserhers hve used S. thunergii s min feed ingredient in lnd-sed intensive ulture systems (Bttglene et l. 1999; Slter et l. 29). However, in our study of vrious experimentl diets, the SGR ws muh higher in se uumers fed UL, LJ, or NO diets ompred to UP, SS, nd ST diets (Fig. 1). Seo et l. (211) reported tht se uumers fed 2% L. jponi nd 2% S. thunergii ontining diet grew muh etter thn those only eting S. thunergii (4%) diet. Zhu et l. (27) lso reported tht the SGR ws inresed signifintly when se uumers were fed U. ltu ompred with S. thunergii nd the SGR of se uumers deresed when they were fed L. jponi. They used muh smller sized (.49 g) se uumers ompred to ours (2.98 g). Different size of se uumer my hve different diet hoie nd nutrition requirement (Yngisw 1998) IR (gg -1 d -1 ) FCE (%) ST UL UP LJ SS NO ST UL UP LJ SS NO Experimentl diets Experimentl diets Fig. 2 Ingestion rte (IR) of Apostihopus jponius fed different test diets. Different letters indite signifint differenes (P <.5) etween tretments within the sme group, nd rs represent stndrd errors Fig. 4 Food onversion effiieny (FCE) of Apostihopus jponius fed different test diets. Different letters indite signifint differenes (P <.5) etween tretments within the sme group, nd rs represent stndrd errors

6 Anisuzzmn et l. Fisheries nd Aquti Sienes (217) 2:24 Pge 6 of 8 Reltive IL-1 gene expression LPS ST UL UP LJ SS NO Diet odes Fig. 5 IL-1 gene expression. IL-1 gene expressions were signifintly inresed y dministrtion of the UL, LJ, nd NO diets Alge re n importnt food soure for se uumers. Zhu et l. (27) reported tht U. ltu s feed ingredient for the se uumers ws etter thn S. thunergii in growth performne. In the present studies, NO, ST, SS, nd UP diets of whih the protein ontents were higher thn those of the UL nd LJ diets were seleted to test the effets on growth of the se uumers (Tle 2). The results showed tht SGR of the se uumers fed the UL nd LJ diets ws signifintly higher thn tht of those fed the ST, SS, nd UP diets. The results indite tht some other ftors were responsile for the nutrient effets of the lge esides the protein, lipid, nd energy ontents. One of the three mehnisms suh s id hydrolysis, enzymti digestion, or mehnil triturtion is neessry to rek the ell wll of mirolgl ell ontents (Bitterlih 1985). For instne, mny fishes like tilpi re the speies whih rely on id hydrolysis. They re le to disrupt ynoterium ell wlls euse of low ph vlues of their stomh fluid (Culton 1976; Pyne 1978). But for holothurins like the se uumer, the struture nd environment of the digestive trt of the se uumer re quite different from tilpi. Se uumers hve no speilized orgn for grinding or glnd for hemil digestion (Mssin 1982), nd digestive enzyme tivities re very low nd hve very little ellulose tivity (Wng et l. 27). Therefore, se uumers re le to ssimilte speifi mount of ellulose ontent. In our studies, the higher SGR of the se uumer ws oserved in the tretments fed with the UL nd LJ diets though the protein nd lipid ontents of those diets were omprtively low (P <.5). UL lge re two ells thik, soft nd trnsluent, nd LJ is multiellulr, filmentous. Their ell wlls re esy to rek nd hve omprtively lower ellulose ontent (Burrows 1991; Miyi et l. 28). So, se uumers ould esily digest nd tke full dvntge of the nutrients in the UL nd LJ lge. The lge UP nd SS ontin signifint mount of ellulose nd need speifi enzyme tivities to rek the ellulose ontent (Jurkovi et l. 1995). Se uumers hve lower speifi enzyme tivities nd my not digest mrolge suh s SS nd UP effiiently (Wng et l. 27). Moreover, Shizohytrium lge hve higher mount of lipids (Menghe et l. 29). But se uumers hve low tolerne to lipids nd do not require high dietry lipid (Seo nd Lee 211). Therefore, in our studies, se uumers fed the UP nd SS diets hd lower SGR mong ll the tretments with the exeption of the ST diets. Ingestion rtes (IRs) of se uumers were signifintly ffeted y different experimentl diets. There ws negtive reltionship etween IR nd the protein level. In the nturl eosystem, low nutritionl vlue of sediment onsumed y deposit feeders mens those nimls need to onsume lrge mounts of sediment in order to otin net input of energy (Sntos et l. 1994; Hudson et l. 24). Vie vers, when food qulity eomes etter, internl ppetite regultion would work tively to derese food ingestion. In this study, the ingestion rte of se uumers deresed when the protein ontent of the diets inresed. The sme phenomenon ws lso found in other ehinoderms. MBride et l. (1998) reported tht for se urhin (Strongyloentrotus frnisnus), prepred diets of different protein levels resulted in different ingestion rte. Otero-Villnuev et l. (24) lso found in Psmmehinus miliris tht the lowest ingestion rte ws relted to high energeti diet. Regultory T ells (Treg ells), known s suppressor T ells, re supopultion of T ells nd modulte the immune systems (Kikodze et l. 216). IL-1 is one of the Treg ells nd known s key regultor of immunity to mny infetions or inflmmtory diseses (Gutierrez- Murgs et l. 216). For instne, high levels of IL-1 hve protetive effet ginst sthm disese (Reiszdeh Jhromi et l. 214). Conversely, lk of IL-1 promotes ell poptosis during virus infetion in the smll intestine (Pn et l. 214). In previous study, we lredy investigted tht dministrtion of se umer totl extrt n upregulte IL-1 nd meliorte sthm disese (Lee et l. 216). Here, we suggest tht UL, LJ, nd NO lge inrese interleukin (IL)-1 gene expression. Conlusions In onlusion, the results of this experiment suggest tht dietry inlusion with Ulv ltu, Lminri jponi, nd Nnnohloropsis oult lge my improve growth of juvenile se uumers nd ould upregulte IL-1 gene expression. Suh detiled informtion ould e helpful in further development of more pproprite diets for the ulture of se uumer.

7 Anisuzzmn et l. Fisheries nd Aquti Sienes (217) 2:24 Pge 7 of 8 Arevitions FCE: Food onversion effiieny; FPR: Fees prodution rte; IL: Interleukin; IR: Ingestion rte; SGR: Speifi growth rte; SR: Survivl rte Aknowledgements This reserh ws prt of the projet titled Feed development for the prodution of se uumer ontins sustne improving sthm meliorted mteril funded y the Ministry of Oens nd Fisheries, Kore. Funding The design of the study; olletion, nlysis, nd interprettion of the dt; nd writing of the mnusript were funded y grnt from the Ministry of Oens nd Fisheries, Kore (215297). Avilility of dt nd mterils All dtsets generted during nd/or nlyzed during the urrent study re ville from the orresponding uthor on resonle request. Authors ontriutions AM, UCJ, nd SJK designed the study. AM wrote the rtile. AM, UCJ, FJ, JKC, nd KK mnuftured the experimentl feed, onduted the feeding tril, nd performed the nlyses. DIL nd HSY performed the interleukin-1 experiment. SJK oneived, oordinted, nd revised the mnusript. All uthors red nd pproved the finl mnusript. Ethis pprovl All experimentl protools followed the guidelines of the Institutionl Animl Cre nd Use Committee of the Pusn Ntionl University nd Gyeongsng Ntionl University. Consent for pulition Not pplile Competing interests The uthors delre tht they hve no ompeting interests. Pulisher s Note Springer Nture remins neutrl with regrd to jurisditionl lims in pulished mps nd institutionl ffilitions. Author detils 1 Deprtment of Sefood nd Aquulture Siene, Gyeongsng Ntionl University, Tongyeong 5364, Repuli of Kore. 2 Deprtment of Prsitology, Shool of Mediine, Pusn Ntionl University, Yngsn-si, Gyeongsngnm-do , Repuli of Kore. Reeived: 16 June 217 Aepted: 11 Septemer 217 Referenes Agtsum Y. Food onsumption nd growth of the juvenile se urhin Strongyloentrotus intermedius. Fish Si. 2;66: Bttglene SC, Seymour EJ, Rmoffi C. Survivl nd growth of ultured juvenile se uumers Holothuri sr. Aquulture. 1999;178: Bitterlih G. Digestive proess in silver rp Hypophthlmihthys molitrix studied in vitro. Aquulture. 1985;5: Bordr S, Anwr F, Sri N. High-vlue omponents nd iotives from se uumers for funtionl foods: review. Mrine Drugs. 211;9: Burrows EM. Seweeds of the British Isles, vol. 2. London: Nturl History Museum; Culton MS. The importne of pre-digestive food preprtion to Tilpi rendlli Boulnger when feeding on quti mrophytes. Trns Rhod Si Asso. 1976;57:22 8. Connd C. Present sttus of world se uumer resoures nd utiliztion: n interntionl overview. Advnes in se uumer quulture nd mngement (Lovtelli, A., Connd,C., Purell, S., Uthike, S., Hmel, J.F. & Merier, A. eds), FAO, Rome, Itly; 24. p Esmt AY, Sid MM, Solimn AA, El-Msry KS, Bdie EA. Biotive ompounds, ntioxidnt potentil, nd heptoprotetive tivity of se uumer (Holothuri tr) ginst thioetmide intoxition in rts. Nutrition. 213;29: Frshdpour F, Ghrii S, Therzdeh M, Amirinejd R, Therkhni R, Hiin A, Zndi K. 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