Evaluating artificial diets for small Paracentrotus lividus (Echinodermata: Echinoidea)
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1 Evaluating artificial diet for mall Paracentrotu lividu (Echinodermata: Echinoidea) Catherine Fernandez, CEVAREN, EqEL, Univerité de Core, & CRITT Core Technologie Corte, France. Charle Françoi Boudoureque UMR DIMAR 3, Faculté de Luminy, Mareille, France. ABSTRACT: Artificial diet are important for ea urchin aquaculture. We tudied growth and nutrition parameter of mall Paracentrotu lividu fed 3 artificial diet. Three different diet type were ued : vegetable-bae type (low protein - high carbohydrate level), mixed-bae type (animal and vegetable) (medium protein and carbohydrate level) or animal-bae type (high protein - low carbohydrate level). We recorded ingetion, aborption, aimilation efficiency and total growth rate. Thee parameter were recorded monthly over a 9 month period from October 1993 to July At the end of the experiment, we alo recorded gonadic, tet, gut and lantern growth rate. Diet type influenced ingetion, aborption, aimilation efficiency and total growth rate. The highet ingetion rate wa obtained with vegetable. The highet aborption rate wa recorded with animal, the lowet with vegetable. Aborption wa negatively correlated with ingetion and carbohydrate level of the food. The aimilation efficiency wa lowet with vegetable diet and highet with animal diet. Growth of tet and gonad wa bet for mall urchin fed mixed diet. INTRODUCTION The world annual conumption of ea urchin ha been teadily increaing over the lat year and many countrie, uch a France, are currently confronted with the problem of over- exploitation of tock. For thi reaon, ea urchin aquaculture eem to be a promiing mean of olving thi problem in the future (Le Gall & Bucaille, 1987). In France recent reearch aim have been directed toward the tudy of Paracentrotu lividu (Lamarck) in order to etablih optimal rearing condition for thi pecie (Le Gall & Bucaille, 1987; Fernandez & Caltagirone, 1994; Grojean & Jangoux, 1994; Fernandez et al., 1995). One of the eential point for the development of ea urchin aquaculture i the availability of an artificial. In nature, Paracentrotu lividu eentially on marine plant although animal material may alo be part of it diet (Neill & Pator, 1973; Verlaque, 1987). In order to maximize the feaibility of ea urchin farming (availability, tocking, etc.), the utilization of artificial eem indipenable. Artificial are uccefully ued elewhere to rear Echinoidea or maintain them in aquaria (Lawrence et al., 1989; 1992; Klinger et al., 1994). It i therefore neceary to undertand how of 651 artificial are utilized by ea urchin. The aim of thi tudy i to monitor parameter of nutrition in mall ized Paracentrotu lividu fed different type of artificial meauring ingetion, aborption, aimilation and growth rate. MATERIALS AND METHODS Sea urchin, Paracentrotu lividu, were collected in the Urbinu lagoon (Corica, France, Mediterranean) in September The ize of the urchin collected wa between and 25 mm (mean ize : 23.2 ± 1.1 mm and mean weight : 5.8 ±.9 g; mean ± tandard deviation). Urchin were maintained in laboratory in three aquaria filled with running water (ambient temperature and alinity between 38 and 39 %). Aquaria were divided into 1 equal compartment and one ea urchin wa placed in each compartment. Urchin were fed artificial during a 9 month period (from October 1t, 1993 to July 1t, 1994). Each group of 1 individual (each aquarium) wa fed a different artificial, which differed in quality and biochemical compoition. The firt conit of vegetable meal and vegetable oil: thi food i rich in oluble carbohydrate (58%) and i refereed to a
2 «vegetable». The econd conit of fih meal and vegetable meal in equal quantitie mixed with fih oil and vegetable oil and i referred to a «mixed food». It biochemical compoition i a mix of oluble protein (29%) and oluble carbohydrate (35%). The third conit of fih meal and fih oil and i rich in oluble protein (47 %) and i referred to a «animal». Sea urchin were alway provided urplu food. Ingetion rate were meaured monthly. Ingetion wa determined over a three day period and for each type, after a given amount of food wa provided every 24h to each urchin. The not ingeted at the end of 24 hour wa collected, freeze dried and weighed. Individual ingetion rate were calculated a the difference between the amount of food available and the amount of food not ingeted (dry weight). In addition, water content and diolution rate of 1 block of were determinated. Thee parameter allowed for an aement of food bioma loe and were ued to correct daily ingetion rate. Aborption rate were alo meaured monthly. Aborption wa determinated by collecting fecal pellet produced by 1 urchin every 24 hour during the 3 day ing period. Food remain, podia and pine were removed from fecal pellet. Pellet were then rined with ditilled water, freeze dried and weighed. Aborption rate were calculated uing the following equation : Aborption rate (%) = (ingeted bioma - defecated bioma) x 1 / (ingeted bioma) Growth wa alo recorded monthly by determinating the total wet weight (after 1 min drainage on paper towel) of each ea urchin. At the end of the experiment the gonad, gut, tet and lantern dry weight for each ea urchin were determined after diection and drying in an oven at 7 C (to a contant weight). Thee meaurement were alo taken at the beginning of the experiment from ten urchin collected at the ame time a the experimental animal. The difference in mean weight for each ea urchin part at the beginning and at the end of the experiment wa ued to etimate growth rate for each organ. From thee data the aimilation rate were calculated uing followed equation: Aimilation rate (%) = Ingetion rate x 1 / growth rate The nutritional budget, in dry weight, were then etablihed from all the data obtained. Thi data i repreented in the format ued by Hawkin & Hartnoll (1983) a modified by Frantzi. After teting the normality of the data and variance homogeneity, the reult were ubjected to one-way or two-way ANOVA, coupled with the Tukey tet (Zar 1984). RESULTS Ingetion The ea urchin' mean ingetion rate (dry weight/day) differed ignificantly depending on the provided and the time of ampling (two way ANOVA, p<.5) (Figure 1). Ingetion rate are highet when ea urchin are fed the vegetable (Tukey tet, p<.5) regardle of the ampling period. Statitical analyi reveal that the ingetion rate i ignificantly and negatively correlated to the protein content of the (r =.55, p<.5) INGESTION RATE (mg dry weight/day) oct-93 nov-93 dec-93 janv-94 feb-94 mar-94 apr-94 may-94 jun-94 Vegetable Mixte Animal Figure 1 : Mean ingetion rate of Paracentrotu lividu fed three type of artificial over a 9 month period. Aborption Aborption efficiency varie ignificantly with type (one way ANOVA, p<.5) (Figure 2). The lowet aborption efficiency i obtained with vegetable, followed by the mixed and finally the highet aborption efficiency i obtained with the animal (Tukey tet, p<.5). Correlation between aborption efficiencie and the level of oluble protein and oluble carbohydrate of the are r =.8 and r = -.81, 652
3 repectively. The higher the protein content, the greater the aborption efficiency. ABSORPTION EFFICIENCY (%) Aimilation Significant difference in gro aimilation efficiencie are oberved for the three type (one-way ANOVA, p<.1). The lowet aimilation efficiencie are oberved for the vegetable. Vegetable alo yield high ingetion rate and low growth rate. Gro aimilation efficiencie are not ignificantly different for individual fed the animal and mixed (Figure 4). % % Vegetable 67% Mixed 76% Animal % GROSS ASSIMILATION EFFICIENCY (%) 1% 18 % % Figure 2 : Mean aborption efficiency (± confidence interval) for Paracentrotu lividu fed three food type. Vegetable Mixed Animal Growth The initial ize of the ea urchin wa 23.2 mm (5.8 g). At the end of the experiment the final ize varied according to the food provided (one-way ANOVA, p<.5) (Figure 3). Maximal growth wa oberved for ea urchin fed either mixed or animal (Tukey tet, p<.5). Reult obtained at the end of the rearing period reveal alo that the gonadal, gut and tet increaed ubtantially during experiment; converely, the lantern decreaed during the nine month of the experiment (two-way ANOVA, p<.5) (Figure 3). Figure 4 : Mean aimilation efficiencie (± confidence interval) for Paracentrotu lividu fed three food type. Organ allocation Aimilated food i allocated firt to tet production, then to gonadic production, to lantern production and finally to gut production, and that for the three food type (two-way ANOVA, p<.5) (Figure 5). 653
4 Tet diameter (mm) Wet weight (g) Indice (% wet weight) Tet Diameter 5 Wet Weight Gonad Gut Lantern Tet Begin of experiment Vegetable Mixed Animal Figure 3 : Mean tet diameter, wet weight and indice (± tandard deviation) for Paracentrotu lividu at the begin of the experiment and at the end of the experiment for the three food type. v : 49.4 % v :.1 % Size -25 mm m : 66.9 % Gut : m :.2 % a : 75.6% a :.2 % Ingeted food v : 34.7 g m : 25.9 g a : 25.6 g Aborption F a e c e v : 5.6 % m : 33.1 % a : 24.4 % L o e v : 41.3 % m : 52.8 % a : 6.5 % Lanterne : Tet : Gonad : v :.7 % m : 1.1 % a : 1.1 % v : 6.5 % m : 1.6 % a : 12.3 % v :.8 % m : 2.3 % a : 1.6 % Figure 5 : Nutritional budget (in dry weight) obtained for mall Paracentrotu lividu over a 9 month period. v : budget obtained with vegetable ; m : budget obtained with mixed, a : budget obtained with animal. Reult of the preent tudy reveal that ingeted food i mainly ued for tet and gonadic growth but that the level allocated to each of thee tiue differ depending on food compoition (two-way ANOVA, p<.5). In particular, we oberved that animal and mixed enhanced tet growth. In addition, the mixed allow an allocation of nutrient to gonadal production (one-way ANOVA, p<.5). Finally, the metabolic activity meaured a lo oberved (allocated to maintenance uch a repiration, excretion and ecretion) are highet with the animal. Thee loe decreae for the mixed and are lowet with the vegetable. DISCUSSION 654 The reult of thi experiment how that food quality influenced ing parameter and growth. For ingetion rate, the influence of food type on thi parameter ha alo been reported for Echinoidea a Strongylocentrotu droebachieni, Strongylocentrotu francicanu or Paracentrotu lividu fed natural eaweed (Vada, 1977; Frantzi, 1992). Thee difference may be due to the characteritic of the food conumed (Paine & Vada, 1969; Frantzi, 1992). In the preent tudy, a ignificant correlation wa een between ingetion rate and protein level. Our data upport the compenatory food intake model which predict an invere relationhip between ingetion rate and food quality (Frantzi, 1992). We oberve an increaed ingetion
5 rate when the level of oluble protein in the food i low (the level of protein being an indication of food quality). Other author have made imilar obervation namely ea urchin inget greater quantitie of low nitrogen food to obtain the protein neceary for their growth and maintenance (Miller & Mann, 1973; Lowe & Lawrence, 1976). For eaonal variation of ingetion rate, imilar obervation have already been oberved for other Echinoidea: Miller & Mann (1973) oberved a ignificant poitive correlation between ingetion rate and water temperature for Strongylocentrotu droebachieni and Fuji (1967) oberved that Strongylocentrotu intermediu very little jut prior to and during it pawn. In the literature, a in our work, aborption efficiencie meaured for Paracentrotu lividu vary according to food type (Lawrence et al. 1989, Frantzi, 1992). Thi lat author obtained aborption efficiencie from 26% for Corallina elongata to 96% for Aparagopi armata. Lawrence et. al. (1989), uing artificial food, obtain value between 8 and 34 %. The difference oberved could be due in part to the containing vegetable meal which are rich in oluble carbohydrate alo contain inoluble carbohydrate. Thee inoluble carbohydrate are not digeted by Echinoidea (Lawrence, 1976) and would therefore lower the aborption efficiency. Invetigation on for other pecie of echinoid, have provided evidence of the effect of food type on growth (Lawrence, 1975 ; Vada, 1977 Laron et al.,198). The good efficiency of contained fih meal in our experiment confirm that P. lividu i omnivorou. The efficiency of an omnivorou diet for ea urchin growth i debated. For Strongylocentrotu droebachieni, experiment uggeted that thi urchin grew fater on a diet of kelp than on diet of only muel (Bricoe & Seben, 1988) but other experiment ugget that mixed diet (kelp with ectoproct) i more efficiency than kelp alone (Netler & Harri, 1994). Our experiment a thee lat experiment ugget that the nutrient available from omnivorou or animal diet allow for optimal growth. Thi i alo true for gro aimilation efficiency. Food compoition generally influence gro aimilation efficiency in Echinoidea (Fuji, 1967; Leighton 1968), the gro aimilation efficiencie obtained with animal and mixed are greater than thoe oberved for ea urchin fed a natural marine plant diet. The poibility exit that aimilation could be improved for artificial diet. 655 Concerning organ allocation, everal experimentation have hown that reource allocation varie under different level of nutrition (Ebert, 1996). Generally, when food i carce, individual allocated relatively more of their available reource to lantern growth (Ebert, 198; Black et al., 1982 ; Levitan 1991) and le to gonad and gut growth (Ebert, 1996). Our reearch alo ugget that the quality of food affect reource allocation. When nutritional value i high (rich in protein), ea urchin allocated relatively more energy to tet and gonad growth than when nutritional value i lower. In concluion, our reult ugget a mixed protein/carbohydrate provide the bet reult with a low ingetion rate and high aborption and gro aimilation efficiencie. Tet and gonad growth were enhanced with the mixed diet. Therefore we recommend thi diet for ea urchin aquaculture. ACKNOWLEDGEMENTS The author wih to thank L. Bronzini de Caraffa, manager of the SCORSA Company, who permitted u to work in the Urbinu lagoon and who provided ea tranportation and to Dr. J. Le Campion, Station Marine d'endoume, for hi help in the tatical apect of thi tudy. Finally, we expre our gratitude to Dr. D. Viale, Univerity of Corica, for providing laboratorie facilitie. REFERENCES Black, R., M.S. Johnon & J.T. Trendal Relative ize of Aritotle' lantern in Echinometra mathaei occuring at different denitie. Mar. Bio.l 71: Bricoe, C.S. & K.P. Seben 1988.Omnivory in Strongylocentrotu droebachieni (Müller) (Echinodermata:Echinoidea) : Predation on ubtidal muel. J. Exp. Mar. Biol. Ecol. 115 :1-24. De Ridder, C. & J.M. Lawrence Food and ing mecanim : Echinoidea. In M. Jangoux & J.M. Lawrence (ed), Echinoderm nutrition: 57-92,
6 Ebert, T.A Relative growth of ea urchin jaw: an example of platic reource allocation. Bull. mar. Sci. 3: Ebert, T.A. 1996, Adaptative apect of phenotypic platicity in echinodrem. Oceanologica acta 19 (3-4): Fernandez, C. & A. Caltagirone Growth rate of adult Paracentrotu lividu in a lagoon environment : the effect of different diet type. In B. David, A. Guille, J.P. Féral & M. Roux (ed), Echinoderm trought time : , Fernandez, C., E. Dombrowki & A. Caltagirone Gonadic growth of adult ea urchin Paracentrotu lividu (Echinodermata : Echinoidea) in rearing : the effect of different diet type. In Emon R., Smith A., Campbell A. (ed), Echinoderm Reearch 1995 : , Rotterdam : Balkema. Frantzi, A Etude expérimentale de niveaux de conommation et d'utiliation de macrophyte et de détritu dérivé par deux invertébré benthique : Paracentrotu lividu (Echinoide, herbivore) et Abra ovata (Bivalve, dépoitivore). Thèe Doct. Océanol., Univ. Aix-Mareille II. Fuji, A Ecological tudie on the growth and food conumption of Japanee common littoral ea urchin Strongylocentrotu intermediu (Agaiz). Mém. Fac. Fih., Univ. Hokkaïdo. 15 (2) : Grojean P. & M. Jangoux, Effect light on ing in cultivated echinoid (Paracentrotu lividu). In B. David, A. Guille, J.P. Féral & M. Roux (ed), Echinoderm trought time : 691, Hawkin, S.J. & R.G. Hartnoll Grazing of intertidal algea by marine invertebrate. Oceanogr. Mar. Biol. Ann. Rev. 21 : Klinger, T.S., J.M. Lawrence & A.L. Lawrence Digetive characteritic of the eaurchin Lytechinu variegatu (Lamarck) (Echinodermata : Echinoidea) fed prepared. J. World aquaculture Soc. 25 (4) : Lawrence, J.M Aborption efficiencie of four pecie of tropical echiniod fed Thalaia tetudinum. Thalaia jugolavica 12 (1) : 1-5. Lawrence, J.M., L.Fenaux, M.C. Corre & A. Lawrence The effect of quantity and quality of prepared diet on production in Paracentrotu lividu (Echinodermata : Echinoidea). In L. Scalera-Liaci & C. Canicatti (ed), Echinoderm Reearch 1991: Lawrence, J.M., M.B. Regi, P. Delma, G. Gra & T. Klinger The effect of quality of food on ind and digetion in Paracentrotu lividu (Lamarck) (Echinodermata: Echinoidea). Mar. Behav. Phyiol. 15: Le gall, P. & D. Bucaille Intérêt d'un élevage intenif de l'ourin violet Paracentrotu lividu. In C.F. Boudoureque (ed), Colloque international ur Paracentrotu lividu et le ourin cometible : Mareille : GIS Poidonie. Leighton, D.L A comparative tudy of food election and nutrition in the abalone Halioti rufecen (Swainon) and the ea urchin Strongylocentrotu purpuratu (Stimpon). Ph D thei, Univ. California. Levitan, D.R Skeletal change in the tet and jaw of the ea urchin Diadema antillarum in repone to food limitation. Mar. Biol. 11 : Lowe, E.F. & J.M. Lawrence Aborption efficiencie of Lytechinu variegatu (Lamarck) (Echinodermata: Echinoidea) for elected marine plant. J. exp. mar. Biol. Ecol. 21: Miller, R.J. & K.H. Mann Ecological energetic of eaweed zone in a marine bay on the Atlantic coat of Canada. III. Energy tranformation by ea urchin. Mar. Biol. 18 : Neill, F.X. & R. Pator Relacione trofica de Paracentrotu lividu (Lmk.) en la zona litoral. Invet. Peq. 37 (1) :1-7. Netler, E.C. & L.G. Harri The importance of omnivory in Strongylocentrotu droebachieni (Müller) in the gulf of Maine. In B. David, A. Guille, J.P. Féral & M. Roux (ed), Echinoderm trought time: , 656
7 Paine, R.T. & R.L. Vada Calorific value of benthic marine algae and their potulated relation to invertabrate food preference. Mar. Biol. 4: Verlaque, M Relation entre Paracentrotu lividu (Lmk.) et le phytobentho de Méditerranée occidentale. In C.F. Boudoureque (ed), Colloque international ur Paracentrotu lividu et le ourin cometible: 5-36, Mareille : GIS Poidonie. Zar, J.H Biotatitical analyi. Prentice-Hall International (ed). 657
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