Echinoderms :San Francisco, Mooi & Telford (eds) © 1998 Balkema, Rotterdam, ISBN 90 5410 929 7
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
small sized Paracentrotus lividus fed different
types of artificial feeds measuring ingestion,
absorption, assimilation and growth rates.
The world annual consumption of sea urchins has
been steadily increasing over the last years and
many countries, such as France, are currently
confronted with the problem of over- exploitation
of stocks. For this reason, sea urchin aquaculture
seems to be a promising means of solving this
problem in the future (Le Gall & Bucaille, 1987). In
France recent research aims have been directed
towards the study of Paracentrotus lividus
(Lamarck) in order to establish optimal rearing
conditions for this species (Le Gall & Bucaille ,
1987; Fernandez & Caltagirone, 1994; Grosjean &
Jangoux, 1994; Fernandez et al., 1995). One of the
essential points for the development of sea urchin
aquaculture is the availability of an artificial feed.
In nature, Paracentrotus lividus feeds essentially on
marine plants although animal material may also be
part of its diet (Neill & Pastor, 1973; Verlaque,
1987). In order to maximize the feasibility of sea
urchin farming (availability, stocking, etc.), the
utilization of artificial feed seems indispensable.
Artificial feeds are successfully used elsewhere to
rear Echinoidea or maintain them in aquaria
(Lawrence et al., 1989; 1992; Klinger et al., 1994).
It is therefore necessary to understand how of
MATERIALS AND METHODS
Sea urchins, Paracentrotus lividus, were collected
in the Urbinu lagoon (Corsica, France,
Mediterranean) in September 1993. The size of the
urchins collected was between 20 and 25 mm
(mean size : 23.2 ± 1.1 mm and mean weight : 5.8
± 0.9 g; mean ± standard deviation). Urchins were
maintained in laboratory in three aquaria filled with
running water (ambient temperature and salinity
between 38 and 39 %). Aquaria were divided into
10 equal compartments and one sea urchin was
placed in each compartment. Urchins were fed
artificial feeds during a 9 month period (from
October 1st, 1993 to July 1st, 1994). Each group of
10 individuals (each aquarium) was fed a different
artificial feed, which differed in quality and
biochemical composition. The first feed consists of
vegetable meal and vegetable oils: this food is rich
in soluble carbohydrates (58%) and is refereed to as
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Echinoderms :San Francisco, Mooi & Telford (eds) © 1998 Balkema, Rotterdam, ISBN 90 5410 929 7
« vegetable feed ». The second feed consists of fish
meal and vegetable meal in equal quantities mixed
with fish oil and vegetable oil and is referred to as
« mixed food ». Its biochemical composition is a
mix of soluble proteins (29%) and soluble
carbohydrates (35%). The third feed consists of fish
meal and fish oil and is rich in soluble proteins (47
%) and is referred to as « animal feed ». Sea urchins
were always provided surplus food.
Ingestion rates were measured monthly. Ingestion
was determined over a three day period and for
each feed type, after a given amount of food was
provided every 24h to each urchin. The feed not
ingested at the end of 24 hours was collected, freeze
dried and weighed. Individual ingestion rates were
calculated as the difference between the amount of
food available and the amount of food not ingested
(dry weight). In addition, water content and
dissolution rates of 10 blocks of feed were
determinated. These parameters allowed for an
assessment of food biomass losses and were used to
correct daily ingestion rates.
Absorption rates were also measured monthly.
Absorption was determinated by collecting fecal
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
calculated using the following equation :
represented in the format used by Hawkins &
Hartnoll (1983) as modified by Frantzis.
Absorption rate (%) = (ingested biomass defecated biomass) x 100 / (ingested biomass)
150
After testing the normality of the data and variance
homogeneity, the results were subjected to one-way
or two-way ANOVA, coupled with the Tukey test
(Zar 1984).
RESULTS
Ingestion
The sea urchins' mean ingestion rates (dry
weight/day) differed significantly depending on the
feed provided and the time of sampling (two way
ANOVA, p<0.05) (Figure 1). Ingestion rates are
highest when sea urchins are fed the vegetable feed
(Tukey test, p<0.05) regardless of the sampling
period. Statistical analysis reveals that the ingestion
rate is significantly and negatively correlated to the
protein content of the feed (r = 0.55, p<0.05).
INGESTION RATE (mg dry weight/day)
250
200
Vegetable feed
100
Mixte feed
50
jun-94
may-94
apr-94
mar-94
feb-94
janv-94
dec-93
Animal feed
nov-93
0
oct-93
Growth was also recorded monthly by
determinating the total wet weight (after 1 min
drainage on paper towel) of each sea urchin. At the
end of the experiment the gonad, gut, test and
lantern dry weights for each sea urchin were
determined after dissection and drying in an oven at
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
weight for each sea urchin part at the beginning and
at the end of the experiment was used to estimate
growth rate for each organ. From these data the
assimilation rates were calculated using followed
equation:
Figure 1 : Mean ingestion rate of Paracentrotus lividus
fed three types of artificial feed over a 9 month period.
Absorption
Absorption efficiency varies significantly with feed
type (one way ANOVA, p<0.05) (Figure 2). The
lowest absorption efficiency is obtained with
vegetable feed, followed by the mixed feed and
finally the highest absorption efficiency is obtained
with the animal feed (Tukey test, p<0.05).
Correlation between absorption efficiencies and the
level of soluble protein and soluble carbohydrates
of the feeds are r = 0.80 and r = - 0.81,
Assimilation rate (%) = Ingestion rate x 100 /
growth rate
The nutritional budgets, in dry weight, were then
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
(Figure 4).
90
80
70
60
50
40
30
20
10
0
GROSS ASSIMILATION EFFICIENCY
(%)
25
49%
67%
76%
20
%
%
ABSORPTION EFFICIENCY (%)
Vegetable
feed
Mixed
feed
15
10
Animal
feed
5
10%
18 %
20%
0
Figure 2 : Mean absorption efficiency (± confidence
interval) for Paracentrotus lividus fed three food types.
Vegetable
feed
Mixed
feed
Animal
feed
Figure 4 : Mean assimilation efficiencies (± confidence
interval) for Paracentrotus lividus fed three food types.
Growth
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
ANOVA, p<0.05) (Figure 3). Maximal growth was
observed for sea urchins fed either mixed or animal
feed (Tukey test, p<0.05). Results obtained at the
end of the rearing period reveal also that the
gonadal, gut and test index increased substantially
during experiment; conversely, the lantern index
decreased during the nine months of the experiment
(two-way ANOVA, p<0.05) (Figure 3).
Organ allocation
Assimilated food is allocated first to test
production, then to gonadic production, to lantern
production and finally to gut production, and that
for the three food types (two-way ANOVA,
p<0.05) (Figure 5).
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Echinoderms :San Francisco, Mooi & Telford (eds) © 1998 Balkema, Rotterdam, ISBN 90 5410 929 7
60
17
34
28
26
24
Indices (% wet weight)
30
Wet weight (g)
Test diameter (mm)
50
15
32
13
11
9
7
22
20
40
30
20
10
5
Test
Diameter
0
Wet
Weight
Begin of experiment
Gonad
index
Vegetable feed
Gut
index
Mixed feed
Lantern
index
Test
index
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 : 34.7 g
m : 25.9 g
a : 25.6 g
Gut :
{
{
{
Ingested food
{
v : 0.1 %
m : 0.2 %
a : 0.2 %
v : 0.7 %
Lanterne :
m : 1.1 %
a : 1.1 %
v : 6.5 %
Test : m : 10.6 %
a : 12.3 %
v : 49.4 %
m : 66.9 %
a : 75.6%
Size 20-25 mm
Absorption
L
o
s
s
e
s
F
a
e
c
e
s
{
{
v : 50.6 %
m : 33.1 %
a : 24.4 %
{
Gonads :
v : 41.3 %
m : 52.8 %
a : 60.5 %
v : 0.8 %
m : 2.3 %
a : 1.6 %
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
that the levels allocated to each of these tissues
differs depending on food composition (two-way
ANOVA, p<0.05). In particular, we observed that
animal and mixed feeds enhanced test growth. In
addition, the mixed feed allows an allocation of
nutrients to gonadal production (one-way ANOVA,
p<0.05). Finally, the metabolic activity measured as
loss observed (allocated to maintenance such as
respiration, excretion and secretion) are highest
with the animal feed. These losses decrease for the
mixed feed and are lowest with the vegetable feed.
The results of this experiment show that food
quality influenced feeding parameters and growth.
For ingestion rate, the influence of food type on this
parameter has also been reported for Echinoidea as
Strongylocentrotus droebachiensis, Strongylocentrotus franciscanus or Paracentrotus lividus fed
natural seaweed (Vadas, 1977; Frantzis, 1992).
These differences may be due to the characteristics
of the foods consumed (Paine & Vadas, 1969;
Frantzis, 1992). In the present study, a significant
correlation was seen between ingestion rate and
protein levels. Our data support the compensatory
food intake model which predicts an inverse
relationship between ingestion rate and food quality
(Frantzis, 1992). We observe an increased ingestion
DISCUSSION
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
food quality). Other authors have made similar
observations namely sea urchins ingest greater
quantities of low nitrogen food to obtain the protein
necessary for their growth and maintenance (Miller
& Mann, 1973; Lowe & Lawrence, 1976). For
seasonal variations of ingestion rate, similar
observations have already been observed for other
Echinoidea: Miller & Mann (1973) observed a
significant positive correlation between ingestion
rate and water temperature for Strongylocentrotus
droebachiensis and Fuji (1967) observed that
Strongylocentrotus intermedius feeds very little just
prior to and during its spawns.
Concerning organ allocation, several experimentations have shown that resource allocation
varies under different level of nutrition (Ebert,
1996). Generally, when food is scarce, individuals
allocated relatively more of their available
resources to lantern growth (Ebert, 1980; Black et
al., 1982 ; Levitan 1991) and less to gonad and gut
growth (Ebert, 1996). Our research also suggests
that the quality of food affect resource allocation.
When nutritional value is high (rich in protein), sea
urchin allocated relatively more energy to test and
gonad growth than when nutritional value is lower.
In conclusion, our results suggest a mixed
protein/carbohydrate feed provides the best results
with a low ingestion rate and high absorption and
gross assimilation efficiencies. Test and gonad
growth were enhanced with the mixed diet.
Therefore we recommend this diet for sea urchin
aquaculture.
In the literature, as in our work, absorption
efficiencies measured for Paracentrotus lividus
vary according to food type (Lawrence et al. 1989,
Frantzis, 1992). This last author obtained
absorption efficiencies from 26% for Corallina
elongata to 96% for Asparagopsis armata.
Lawrence et. al. (1989), using artificial foods,
obtain values between 8 and 34 %. The differences
observed could be due in part to the feeds
containing vegetable meal which are rich in soluble
carbohydrates also contain insoluble carbohydrates.
These insoluble carbohydrates are not digested by
Echinoidea (Lawrence, 1976) and would therefore
lower the absorption efficiency.
ACKNOWLEDGEMENTS
The authors wish to thank L. Bronzini de Caraffa,
manager of the SCORSA Company, who permitted
us to work in the Urbinu lagoon and who provided
sea transportation and to Dr. J. Le Campion, Station
Marine d'Endoume, for his help in the stastical
aspects of this study. Finally, we express our
gratitude to Dr. D. Viale, University of Corsica, for
providing laboratories facilities.
Investigations on for other species of echinoids,
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
fish meal in our experiment confirm that P. lividus
is omnivorous. The efficiency of an omnivorous
diet for sea urchin growth is debated. For
Strongylocentrotus droebachiensis, experiments
suggested that this urchin grew faster on a diet of
kelp than on diet of only mussel (Briscoe & Sebens,
1988) but other experiments suggest that mixed diet
(kelp with ectoproct) is more efficiency than kelp
alone (Nestler & Harris, 1994). Our experiment as
these last experiments suggest that the nutrients
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
assimilation efficiencies obtained with animal and
mixed feeds are greater than those observed for sea
urchins fed a natural marine plant diet. The
possibility exist that assimilation
could be
improved for artificial diets.
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