Evaluating Artificial Diets for Small Paracentrotus Lividus (Echinodermata: Echinoidea)

Evaluating artificial diets for small Paracentrotus lividus (Echinodermata: Echinoidea)

Catherine Fernandez, CEVAREN, EqEL, Université de Corse, & CRITT Corse Technologie Corte, France. Charles François Boudouresque UMR DIMAR 3, Faculté de Luminy, Marseille, France.

ABSTRACT: Artificial diets are important for sea urchin aquaculture. We studied growth and nutrition parameters of small Paracentrotus lividus fed 3 artificial diets. Three different diet types were used : “vegetable-base” type (low protein - high carbohydrate level), “mixed-base” type (animal and vegetable) (medium protein and carbohydrate level) or “animal-base” type (high protein - low carbohydrate level). We recorded ingestion, absorption, assimilation efficiency and total growth rate. These parameters were recorded monthly over a 9 month period from October 1993 to July 1994. At the end of the experiment, we also recorded gonadic, test, gut and lantern growth rate. Diet type influenced ingestion, absorption, assimilation efficiency and total growth rates. The highest ingestion rate was obtained with vegetable feed. The highest absorption rate was recorded with animal feed, the lowest with vegetable feed. Absorption was negatively correlated with ingestion and carbohydrate level of the food. The assimilation efficiency was lowest with vegetable diet and highest with animal diet. Growth of test and gonad was best for small urchins fed mixed diet.

INTRODUCTION artificial feeds are utilized by sea urchins. The aim of this study is to monitor parameters of nutrition in The world annual consumption of sea urchins has small sized Paracentrotus lividus fed different been steadily increasing over the last years and types of artificial feeds measuring ingestion, many countries, such as France, are currently absorption, assimilation and growth rates. confronted with the problem of over- exploitation of stocks. For this reason, sea urchin aquaculture seems to be a promising means of solving this MATERIALS AND METHODS problem in the future (Le Gall & Bucaille, 1987). In France recent research aims have been directed Sea urchins, Paracentrotus lividus, were collected towards the study of Paracentrotus lividus in the Urbinu lagoon (Corsica, France, (Lamarck) in order to establish optimal rearing Mediterranean) in September 1993. The size of the conditions for this species (Le Gall & Bucaille , urchins collected was between 20 and 25 mm 1987; Fernandez & Caltagirone, 1994; Grosjean & (mean size : 23.2 ± 1.1 mm and mean weight : 5.8 Jangoux, 1994; Fernandez et al., 1995). One of the ± 0.9 g; mean ± standard deviation). Urchins were essential points for the development of sea urchin maintained in laboratory in three aquaria filled with aquaculture is the availability of an artificial feed. running water (ambient temperature and salinity In nature, Paracentrotus lividus feeds essentially on between 38 and 39 %). Aquaria were divided into marine plants although animal material may also be 10 equal compartments and one sea urchin was part of its diet (Neill & Pastor, 1973; Verlaque, placed in each compartment. Urchins were fed 1987). In order to maximize the feasibility of sea artificial feeds during a 9 month period (from urchin farming (availability, stocking, etc.), the October 1st, 1993 to July 1st, 1994). Each group of utilization of artificial feed seems indispensable. 10 individuals (each aquarium) was fed a different Artificial feeds are successfully used elsewhere to artificial feed, which differed in quality and rear Echinoidea or maintain them in aquaria biochemical composition. The first feed consists of (Lawrence et al., 1989; 1992; Klinger et al., 1994). vegetable meal and vegetable oils: this food is rich It is therefore necessary to understand how of in soluble carbohydrates (58%) and is refereed to as 651 Echinoderms :San Francisco, Mooi & Telford (eds) © 1998 Balkema, Rotterdam, ISBN 90 5410 929 7

« vegetable feed ». The second feed consists of fish represented in the format used by Hawkins & meal and vegetable meal in equal quantities mixed Hartnoll (1983) as modified by Frantzis. with fish oil and vegetable oil and is referred to as « mixed food ». Its biochemical composition is a After testing the normality of the data and variance mix of soluble proteins (29%) and soluble homogeneity, the results were subjected to one-way carbohydrates (35%). The third feed consists of fish or two-way ANOVA, coupled with the Tukey test meal and fish oil and is rich in soluble proteins (47 (Zar 1984). %) and is referred to as « animal feed ». Sea urchins RESULTS were always provided surplus food. Ingestion rates were measured monthly. Ingestion was determined over a three day period and for Ingestion each feed type, after a given amount of food was provided every 24h to each urchin. The feed not The sea urchins' mean ingestion rates (dry ingested at the end of 24 hours was collected, freeze weight/day) differed significantly depending on the dried and weighed. Individual ingestion rates were feed provided and the time of sampling (two way calculated as the difference between the amount of ANOVA, p<0.05) (Figure 1). Ingestion rates are food available and the amount of food not ingested highest when sea urchins are fed the vegetable feed (dry weight). In addition, water content and (Tukey test, p<0.05) regardless of the sampling dissolution rates of 10 blocks of feed were period. Statistical analysis reveals that the ingestion determinated. These parameters allowed for an rate is significantly and negatively correlated to the assessment of food biomass losses and were used to protein content of the feed (r = 0.55, p<0.05). correct daily ingestion rates. Absorption rates were also measured monthly. Absorption was determinated by collecting fecal INGESTION RATE (mg dry weight/day) pellets produced by 10 urchins every 24 hours during the 3 day feeding period. Food remains, podia and spines were removed from fecal pellets. Pellets were then rinsed with distilled water, freeze dried and weighed. Absorption rates were 250 calculated using the following equation : 200

150 Absorption rate (%) = (ingested biomass - Vegetable feed 100 defecated biomass) x 100 / (ingested biomass) Mixte feed 50 Animal feed Growth was also recorded monthly by 0 determinating the total wet weight (after 1 min oct-93 feb-94 jun-94 dec-93 apr-94 drainage on paper towel) of each sea urchin. At the nov-93 mar-94 may-94 end of the experiment the gonad, gut, test and janv-94 lantern dry weights for each sea urchin were Figure 1 : Mean ingestion rate of Paracentrotus lividus determined after dissection and drying in an oven at fed three types of artificial feed over a 9 month period. 70° C (to a constant weight). These measurements were also taken at the beginning of the experiment from ten urchins collected at the same time as the experimental animals. The difference in mean Absorption weight for each sea urchin part at the beginning and at the end of the experiment was used to estimate Absorption efficiency varies significantly with feed growth rate for each organ. From these data the type (one way ANOVA, p<0.05) (Figure 2). The assimilation rates were calculated using followed lowest absorption efficiency is obtained with equation: vegetable feed, followed by the mixed feed and finally the highest absorption efficiency is obtained Assimilation rate (%) = Ingestion rate x 100 / with the animal feed (Tukey test, p<0.05). growth rate Correlation between absorption efficiencies and the level of soluble protein and soluble carbohydrates The nutritional budgets, in dry weight, were then of the feeds are r = 0.80 and r = - 0.81, established from all the data obtained. This data is 652 Echinoderms :San Francisco, Mooi & Telford (eds) © 1998 Balkema, Rotterdam, ISBN 90 5410 929 7

respectively. The higher the protein content, the greater the absorption efficiency. Assimilation

Significant differences in gross assimilation efficiencies are observed for the three feed types (one-way ANOVA, p<0.0001). The lowest assimilation efficiencies are observed for the vegetable feed. Vegetable feeds also yield high ingestion rates and low growth rates. Gross assimilation efficiencies are not significantly different for individuals fed the animal and mixed ABSORPTION EFFICIENCY (%) (Figure 4).

90 80 70 GROSS ASSIMILATION EFFICIENCY 60 (%) 50 25 % 40 76% 30 67% 20 20 49% 10 15

0 % 10 20% Vegetable Mixed Animal 18 % feed feed feed 5 10%

Figure 2 : Mean absorption efficiency (± confidence 0 interval) for Paracentrotus lividus fed three food types. Vegetable Mixed Animal feed feed feed

Growth Figure 4 : Mean assimilation efficiencies (± confidence interval) for Paracentrotus lividus fed three food types. The initial size of the sea urchins was 23.2 mm (5.8 g). At the end of the experiment the final size varied according to the food provided (one-way Organ allocation ANOVA, p<0.05) (Figure 3). Maximal growth was observed for sea urchins fed either mixed or animal Assimilated food is allocated first to test feed (Tukey test, p<0.05). Results obtained at the production, then to gonadic production, to lantern end of the rearing period reveal also that the production and finally to gut production, and that gonadal, gut and test index increased substantially for the three food types (two-way ANOVA, during experiment; conversely, the lantern index p<0.05) (Figure 5). decreased during the nine months of the experiment (two-way ANOVA, p<0.05) (Figure 3).

60 17 34 15 50 32

30 13 40

28 11 30 26 9 20 24 Wet weight (g) Test diameter (mm)

7 Indices (% wet weight) 22 10

20 5 0 Test Wet Gonad Gut Lantern Test Diameter Wei ght index index index index

Begin of experiment Vegetable feed Mixed feed Animal feed

Figure 3 : Mean test diameter, wet weight and indices (± standard deviation) for Paracentrotus lividus at the begin of the experiment and at the end of the experiment for the three food types.

v : 49.4 % v : 0.1 % Size 20-25 mm m : 66.9 % Gut :{ m : 0.2 % a : 75.6% a : 0.2 % v : 0.7 % { Ingested food Absorption Lanterne :{ m : 1.1 %

{ a : 1.1 % F L v : 6.5 % a o v : 34.7 g Test : m : 10.6 % m : 25.9 g e s c s { a : 12.3 % a : 25.6 g e e s s v : 0.8 % { { Gonads : m : 2.3 % { a : 1.6 % v : 50.6 % v : 41.3 % m : 33.1 % m : 52.8 % a : 24.4 % a : 60.5 %

Figure 5 : Nutritional budgets (in dry weight) obtained for small Paracentrotus lividus over a 9 month period. v : budget obtained with vegetable feed; m : budget obtained with mixed feed, a : budget obtained with animal feed.

Results of the present study reveal that ingested food is mainly used for test and gonadic growth but The results of this experiment show that food that the levels allocated to each of these tissues quality influenced feeding parameters and growth. differs depending on food composition (two-way ANOVA, p<0.05). In particular, we observed that For ingestion rate, the influence of food type on this animal and mixed feeds enhanced test growth. In parameter has also been reported for Echinoidea as addition, the mixed feed allows an allocation of Strongylocentrotus droebachiensis, Strongylocen- nutrients to gonadal production (one-way ANOVA, trotus franciscanus or Paracentrotus lividus fed p<0.05). Finally, the metabolic activity measured as natural seaweed (Vadas, 1977; Frantzis, 1992). loss observed (allocated to maintenance such as These differences may be due to the characteristics respiration, excretion and secretion) are highest of the foods consumed (Paine & Vadas, 1969; with the animal feed. These losses decrease for the Frantzis, 1992). In the present study, a significant mixed feed and are lowest with the vegetable feed. correlation was seen between ingestion rate and protein levels. Our data support the compensatory food intake model which predicts an inverse DISCUSSION relationship between ingestion rate and food quality (Frantzis, 1992). We observe an increased ingestion 654 Echinoderms :San Francisco, Mooi & Telford (eds) © 1998 Balkema, Rotterdam, ISBN 90 5410 929 7

rate when the level of soluble proteins in the food is low (the level of proteins being an indication of Concerning organ allocation, several experi- food quality). Other authors have made similar mentations have shown that resource allocation observations namely sea urchins ingest greater varies under different level of nutrition (Ebert, quantities of low nitrogen food to obtain the protein 1996). Generally, when food is scarce, individuals necessary for their growth and maintenance (Miller allocated relatively more of their available & Mann, 1973; Lowe & Lawrence, 1976). For resources to lantern growth (Ebert, 1980; Black et seasonal variations of ingestion rate, similar al., 1982 ; Levitan 1991) and less to gonad and gut observations have already been observed for other growth (Ebert, 1996). Our research also suggests Echinoidea: Miller & Mann (1973) observed a that the quality of food affect resource allocation. significant positive correlation between ingestion When nutritional value is high (rich in protein), sea rate and water temperature for Strongylocentrotus urchin allocated relatively more energy to test and droebachiensis and Fuji (1967) observed that gonad growth than when nutritional value is lower. Strongylocentrotus intermedius feeds very little just prior to and during its spawns. In conclusion, our results suggest a mixed protein/carbohydrate feed provides the best results In the literature, as in our work, absorption with a low ingestion rate and high absorption and efficiencies measured for Paracentrotus lividus gross assimilation efficiencies. Test and gonad vary according to food type (Lawrence et al. 1989, growth were enhanced with the mixed diet. Frantzis, 1992). This last author obtained Therefore we recommend this diet for sea urchin absorption efficiencies from 26% for Corallina aquaculture. elongata to 96% for Asparagopsis armata. Lawrence et. al. (1989), using artificial foods, ACKNOWLEDGEMENTS obtain values between 8 and 34 %. The differences observed could be due in part to the feeds The authors wish to thank L. Bronzini de Caraffa, containing vegetable meal which are rich in soluble manager of the SCORSA Company, who permitted carbohydrates also contain insoluble carbohydrates. us to work in the Urbinu lagoon and who provided These insoluble carbohydrates are not digested by sea transportation and to Dr. J. Le Campion, Station Echinoidea (Lawrence, 1976) and would therefore Marine d'Endoume, for his help in the stastical lower the absorption efficiency. aspects of this study. Finally, we express our gratitude to Dr. D. Viale, University of Corsica, for Investigations on for other species of echinoids, providing laboratories facilities. have provided evidence of the effect of food type on growth (Lawrence, 1975 ; Vadas, 1977 Larson et al.,1980). The good efficiency of feeds contained REFERENCES fish meal in our experiment confirm that P. lividus is omnivorous. The efficiency of an omnivorous Black, R., M.S. Johnson & J.T. Trendal 1982. diet for sea urchin growth is debated. For Relative size of Aristotle's lantern in Strongylocentrotus droebachiensis, experiments Echinometra mathaei occuring at different suggested that this urchin grew faster on a diet of densities. Mar. Bio.l 71: 101-106. kelp than on diet of only mussel (Briscoe & Sebens, Briscoe, C.S. & K.P. Sebens 1988.Omnivory in 1988) but other experiments suggest that mixed diet Strongylocentrotus droebachiensis (Müller) (kelp with ectoproct) is more efficiency than kelp (Echinodermata:Echinoidea) : Predation on alone (Nestler & Harris, 1994). Our experiment as subtidal mussels. J. Exp. Mar. Biol. Ecol. these last experiments suggest that the nutrients 115 :1-24. available from omnivorous or animal diet allow for optimal growth. This is also true for gross assimilation efficiency. Food composition generally influences gross assimilation efficiency in Echinoidea (Fuji, 1967; Leighton 1968), the gross De Ridder, C. & J.M. Lawrence 1982. Food and assimilation efficiencies obtained with animal and feeding mecanisms : Echinoidea. In M. mixed feeds are greater than those observed for sea Jangoux & J.M. Lawrence (eds), Echinoderm urchins fed a natural marine plant diet. The nutrition: 57-92, Rotterdam: Balkema. possibility exist that assimilation could be improved for artificial diets. 655 Echinoderms :San Francisco, Mooi & Telford (eds) © 1998 Balkema, Rotterdam, ISBN 90 5410 929 7

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