urchins, paracentrotus li idus / lamarck / echinodermatadirectory.umm.ac.id/data...

Ž .Aquaculture 185 2000 85–99www.elsevier.nlrlocateraqua-online

Optimization of gonad growth by manipulation oftemperature and photoperiod in cultivated sea

ž /urchins, Paracentrotus liÕidus Lamarckž /Echinodermata

Christine Spirlet a,b,), Philippe Grosjean a, Michel Jangoux a,b,c

a Laboratoire de Biologie Marine CP 160r15, UniÕersite Libre de Bruxelles, 50 AÕ. F.D. RooseÕelt, B-1050´Brussels, Belgium

b Centre regional d’etudes cotieres, UniÕersite de Caen, Station marine, B.P. 49,´ ´ ˆ ` ´F-14530 Luc-sur-Mer, France

c Laboratories de Biologie Marine, UniÕersite de Mons-Hainaut, 19 rue Maistriau, B-7000 Mons, Belgium´

Accepted 20 October 1999

Abstract

A starvation and then feeding method was developed to produce about 100% marketable seaurchins, Paracentrotus liÕidus, in 3 1r2 months. This method is needed because the reproductioncycle is desynchronized in the conditions imposed during the somatic growth stage in land-basedclosed systems. The major advantages of starving the animals are resetting the reproductive cycle

Ž .to the spent stage gonads almost devoid of sexual cells and stressing the individuals so that theymobilize and restore the nutritive phagocytes, filling them with nutrients. Batches of sea urchinsstarved 2 months beforehand were fed ad libitum for 45 days with enriched food under eight

Ž . Žcombinations of four temperatures 128C, 168C, 208C and 248C and two photoperiods 9 and 17 h.daylight . In our system, the best combination was 248C and 9 h daylight for growth as well as for

Ž .gonad quality. The gonadal indices obtained in dry weight were over 9% at 168C and over 12%at 248C, which are better than what is found in the field for this population. q 2000 ElsevierScience B.V. All rights reserved.

Keywords: Gonad; Growth; Temperature; Photoperiod; Sea urchin; Paracentrotus liÕidus

) Corresponding author. Laboratoire de Biologie Marine Pentagone-Universite de Mons-Hainaut, Avenue du´Champ de Mars 6, B-7000 Mons, Belgium. Tel.: q32-65-373441; fax: q32-65-373434.

Ž .E-mail address: [email protected] C. Spirlet .

0044-8486r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.Ž .PII: S0044-8486 99 00340-3

( )C. Spirlet et al.rAquaculture 185 2000 85–9986

1. Introduction

Increasing demand for sea urchin roe has led in the last decade to over-fishing naturalŽ .populations Conand and Sloan, 1989; Le Gall, 1990 . Several possible solutions have

Žbeen tested: reseeding natural habitats with farmed juveniles Agatsuma and Momma,. Ž1988; Gomez et al., 1995 ; mariculture Fernandez and Caltagirone, 1994; Fernandez,

. Ž1996 ; raising sea urchins in immerged cages, alone Fernandez, 1996; Robinson and. ŽColborne, 1998 ; or with other animals polyculture with salmons notably, Kelly et al.,

.1998 ; and finally land-based, closed-system echiniculture allowing control of eachŽphase of the echinoid biological cycle Le Gall and Bucaille, 1989; Le Gall, 1990;

.Grosjean et al., 1998 .Whatever the culture method, temperate sea urchins exposed to natural conditions of

temperature and photoperiod have a seasonal sexual cycle that restrains the crop to onlyŽ2 or 3 months per year Byrne, 1990; Lozano et al., 1995; Fernandez, 1996; Spirlet et

.al., 1998a . Many experimental attempts have already been made to manipulate thegonadal cycle by modifying these exogenous parameters. Most of them were successful

Žin obtaining out-of-season gametogenesis Leahy et al., 1981; Pearse et al., 1986;.McClintock and Watts, 1990; Walker and Lesser, 1998 . However, the experiments were

always run on specimens collected from the field, and hence, sexually in phase to beginŽwith. Moreover, the shift in the reproductive cycle took at least 7 months Walker and

.Lesser, 1998 .Ž .With adult sea urchins originating from cultivation see Grosjean et al., 1998 , the

first problem is to obtain individuals in phase with regard to their reproductive cycle. Asgonads also act as storage organs, it is possible to induce the consumption of most of

Ž .their content by starving the animal Lawrence, 1985; Pearse and Cameron, 1991 . ThisŽ .attribute, experimentally observed, was successfully used by Spirlet et al. 1998b to

study the impact of feeding strategies on gonadal production and to obtain marketableŽ .sea urchins all year long see Grosjean et al., 1998 . However, it has not been used yet

Žto determine the best values of exogenous parameters mainly, temperature and photope-.riod for optimizing the production of marketable gonads.

Several criteria have to be considered in echiniculture. The reproductive state of thegonads has to be in the correct range, from stage 3 to stage 5 according to Spirlet et al.Ž .1998a ; the gonads preferably need to be fleshy and firm without an abundance ofgametes spilling when they are consumed; and, as previously stated, they also need to besexually synchronized to ensure a large quantity of exploitable individuals all at once.

Ž .This study has two objectives: 1 to determine the influence of the two major abioticŽ .parameters temperature and photoperiod on gonadal growth and gametogenesis of

Ž .cultured sea urchins in a closed-circuit facility; and 2 to control the reproductive cycleand determine the best combination of temperature and photoperiod to obtain individualsready for marketing as soon as possible.

2. Material and methods

The Paracentrotus liÕidus used were laboratory reared from two successive fertiliza-Ž .tions Le Gall and Bucaille, 1989; Grosjean et al., 1996, 1998 . The original stock was

( )C. Spirlet et al.rAquaculture 185 2000 85–99 87

Ž .collected on the rocky shore of Morgat Brittany, France . The individuals selected wereŽ . Ž .30"2 mm "SE of ambital diameter excluding spines and aged 2 years and 3

months at the beginning of the experiment. Indeed, this size class presents the bestŽ .gonadal index GI and therefore, a priori, the best potential of growth for the gonads

Ž .Jangoux et al., 1996 .The experiment was conducted in four specific rearing structures described by

Ž .Grosjean et al. 1998 . They consisted of three superposed toboggans overhanging aŽreserversettling tank. These experimental structures were thermoregulated one tempera-

.ture per unit and each toboggan was isolated so that photoperiod regulation wasindependent. A centrifugal pump insured circulation of the water. A water renewal of200% per day maintained seawater quality during the experiment.

ŽSea urchins were starved 2 months beforehand i.e., until most of the nutrients.present in the gonads were resorbed to make sure they were sexually in phase at the

beginning of the experiment. Starvation occurred at the lowest temperature used in theŽ . Ž .study 128C , to prevent subsequent mortality Jangoux et al., 1996 .

Before initiating the experiment, five batches of six individuals were weighed inŽ .water immersed weight, IW, see below and dissected for control measurements. The

Ž .immersed weighed was then standardized Jangoux et al., 1996, Grosjean et al., 1999 asshown in Eq. 1:

2.80y1.00SIWs IW 1Ž .ž /2.80yMdr1000

with SIW being the standard immersed weight in g, Md the water mass density in grl,estimated from sea water temperature and salinity at the time of measurement and 2.80

Žthe mean density of the sea urchin test allometry between the IW and the dry weight ofthe skeleton calculated on 356 reared animals after digestion of the soft tissues with

.sodium hypochloride 10% under gentle agitation .The gonads were extracted and fresh weighed. One was fixed in Bouin’s fluid to be

analyzed histologically, while the remaining gonads were dried for 48 h at 708C and dryweighed. The value was corrected for the missing gonad.

ŽFor the experiment, eight further sets of 30 individuals five replicates of six.individuals were subjected for 45 days to eight treatments involving combinations

Ž . Žbetween four temperatures 128C, 168C, 208C and 248C and two photoperiods 7 h days.or short day period, SD; 17 h days or long day period, LD . Initial immersed weights

were determined for each batch. From the first day on, the individuals were fed adŽ .libitum with extruded food, in the form of cylindrical pellets 8=15 mm . This food

Žcontained mainly wheat, fish, soybean, and minerals see Klinger et al., 1998 for exact.composition . New food was distributed every other day after leftovers from the

previous distribution were collected. The latter were dried and weighed to estimate theŽ .quantity of ingested food ingestion rate . Additional portions of food were placed in the

same experimental structures, but away from the echinoids, and treated similarly toestimate the loss due to their degradation in seawater. The total ingested food wascalculated with Eq. 2:

FskÝP yÝL 2Ž .i i


with P being the portions distributed, L the leftovers, and k a correction factor thatŽtakes into account the partial degradation of the food in the water k was estimated for

.each treatment .At the end of the experiment, the immersed weight of the echinoids was determined

Ž .prior to dissection. Somatic growth SG was calculated as the difference between theinitial and final dry weights. The initial dry weight was estimated from initial standard

Ž .immersed weight IW . Eq. 3 shows the relationship between the SIW and the dryŽ .weight of soma Grosjean et al., 1999 is:

DW s 1.68=SIW q0.21 3Ž . Ž .soma

where DW is expressed in g of dry weight and SIW is in g.somaŽ .The gonadal growth GG in g of dry weight was assessed as the difference between

the final measured value and the initial value estimated from the control batch andcorrected by the following calculation in Eq. 4:

GWbGW s SIW 4Ž .iniŽest. iniSIWb

where GW and SIW are the values for the measured initial batch, SIW and GWb b ini iniŽest.is the estimated dry weight of the gonads in g when feeding starts.

Ž .Hence, GG is calculated as follows Eq. 5 :

GGsGW yGW 5Ž .fin iniŽest. .

The differential allocation of resources to soma and gonads is evaluated by means ofŽ .the final GI expressed in dry weight Eq. 6 :

GWGI s =100 6Ž .d SWqGW

where GI is the gonadal index in dry weight in percent, GW is the dry weight of thedŽ . Ž .gonads g and SW is the dry weight of the soma g . To compare with other studies,

Ž . Ž .wet weight of gonadal index GI is also evaluated Eq. 7 :w

GWwGI s =100. 7Ž .w TFW

With GI being the gonadal index in fresh weight in percent, GW being the freshw w

weight of the gonads in g and TFW being the total fresh weight of the sea urchin also ing. As a reminder, total fresh weight is independent of the fresh weight of gonads sincethe volume unoccupied by the gonads is replaced by coelomic fluid of equal densitywhile total animal volume does not change. As the SIW is independent of the gonadweight and much more accurate than fresh weight, the TFW is evaluated from the

Ž .allometric relationship presented as Eq. 8 Grosjean et al., in press :

TFWs4.95SIW1.05 . 8Ž .


Ž .Fig. 1. Complete gametogenic cycle of P. liÕidus. In closed-circuit cultivation standard conditions , thegrowing phase circled by a dotted line is actually by-passed: the gonads tend to start gametogenesis directlyonce they have enough nutrients, storing them only occasionally.

The maturity stages were diagnosed by histology and classified following an eightŽ . Ž . Ž .stage scale Spirlet et al., 1998a . The maturity index MI Eq. 9 of a batch was

calculated as:

8

w xMIs C n rn 9Ž .Ý i i1

with C the maturity coefficient going from 1 to 8, n the number of individualsi i

presenting that coefficient, and n the total number of individuals in the batch.

Table 1P. liÕidus. Two-way ANOVA analysis of the effect of temperature and photoperiod on somatic growth,gonadal growth and food ingestion

SS df F-ratio P

Gonadal growthTemperature 44.400 3 66.313 -0.001Photoperiod 0.736 1 3.299 0.079Temperature=Photoperiod 4.004 3 5.980 0.002Error 7.142 32

Somatic growthTemperature 73.123 3 53.857 -0.001Photoperiod 2.473 1 5.464 0.026Temperature=Photoperiod 3.268 3 2.407 0.085Error 14.483 32

Food ingestionTemperature 537.452 3 34.477 -0.001Photoperiod 0.335 1 0.064 0.801Temperature=Photoperiod 37.904 3 2.431 0.083Error 166.281 32


As no difference was noted between males and females in previous studies on wildŽ .populations of P. liÕidus in Morgat Spirlet et al., 1998a and cultivated specimens

Ž . Žpersonal observation , the data were pooled in all analysis Mann–Whitney U-test,.Ps0.05 .

The treatments and the effect of temperature and photoperiod were compared usingŽ .two-way ANOVA and Tukey test for temperature t-test for photoperiod , food inges-

tion, for somatic production and gonadal growth. Normality and uniformity of varianceswere ensured, respectively, by x 2 and Bartlett’s test. As distributions were sometimesasymmetrical and could not always be considered normal, one-way Kruskal–Wallis andMann–Whitney non-parametrical U-tests were more appropriate for the gonad index

Table 2P. liÕidus. Kruskal–Wallis and Mann–Whitney U non-parametrical tests of the effects of temperature andphotoperiod on gonad water content, GI in dry weight and GI in fresh weight

Water content2Photoperiod n Rank sum Mann–Whitney U-test P x approximately df

SD 20 376 234 0.358 0.846 1LD 20 444 234 0.358 0.846 1

Ž .Temperature 8C n Rank sum Kruskal–Wallis test P df

12 10 344 31.26 -0.001 316 10 231 31.26 -0.001 320 10 190 31.26 -0.001 324 10 55 31.26 -0.001 3

Ž .GI dry weight2Photoperiod n Rank sum Mann–Whitney U-test P x approximately df

SD 20 443 167 0.372 0.797 1LD 20 377


12 10 56 30.069 -0.001 316 10 224 30.069 -0.001 320 10 199 30.069 -0.001 324 10 341 30.069 -0.001 3

Ž .GI fresh weight2Photoperiod n Rank sum Mann–Whitney U-test P x approximately df

SD 20 406 204 0.914 0.012 1LD 20 414 204 0.914 0.012 1


12 10 58 22.594 -0.001 316 10 275 22.594 -0.001 320 10 217 22.594 -0.001 324 10 270 22.594 -0.001 3


Ž . 2 Ž .GI . Watson’s U -test was used for the polar transformed values of MI Zar, 1996 .The factor we defined as ‘‘temperature’’ is in fact the combined effect of temperature

Ž .and rearing structure. Indeed, the number of structures available four did not permitreplicates. Thus, although the structures were identical and the seawater was the same,the effect of temperature cannot be technically dissociated from a possible effect of thestructures.

3. Results

ŽObservations of several cohorts of P. liÕidus specimens in culture i.e., follow-up of.gonad growth and MIs, unpublished data led us to the conclusion that gametogenesis

Žwas continuous. In addition, the lack of variation in the external parameters i.e.,.absence of seasonality causes the growth phase to be by-passed as shown in Fig. 1.

Consequently, the gonads are poor in stored nutrients. Finally, the individuals are notsexually synchronized.

Statistical analyses of the results are presented in Tables 1 and 2. The quantity ofŽfood ingested during the experiment was homogeneous for the higher temperatures Fig.

.2 . Only at the 128C treatments did the animals show significantly lower feeding. For theŽ .128C treatments, individuals exposed to the SD treatment winter photoperiod ate less

Ž . Ž .than those exposed to LD summer photoperiod . For higher temperatures over 128C ,ingestion was similar for all treatments.

Fig. 2. P. liÕidus. Food ingestion vs. temperature and photoperiod. Bold horizontal lines at the same levelmean no significant difference.


The results of somatic and gonadal growth are reported in Fig. 3. Somatic growth wasŽ .very low at 128C and increased significantly with temperature Fig. 3a . The somatic

growth was also affected by photoperiod: SD condition at 168C and at 248C gave abetter growth than the LD condition. Likewise, the growth of gonads was positivelyrelated to temperature: gonadal growth was significantly lower at 128C and significantly

Ž . Ž .Fig. 3. P. liÕidus. Mean values of the a somatic production and b gonadal production vs. temperature andphotoperiod. Bold horizontal lines at the same level mean no significant difference.


Fig. 4. P. liÕidus. Mean values of GI calculated in fresh and dry weight vs. temperature and photoperiod. Boldhorizontal lines at the same level mean no significant difference.

Ž .higher at 248C with no difference between 168C and 208C Fig. 3b . Difference betweenphotoperiod regimes was significant only at 248C: gonadal production was more

Žimportant for the SD treatment. Fig. 4 presents final values of GI dry weight GI-DW.and fresh weight GI-FW . The GI was significantly lower at 128C and higher at 248C,

while 168C and 208C were equivalent for both fresh and dry weight measurements. Forthe SD-248C treatment, the GI-DW was unexpectedly superior to the GI-FW. This result

Ž .led us to assess the mean water content of the gonads expressed in percent and allowedus to note an effective change in that parameter depending upon treatments. The data arereported in Table 3. Water content and temperature were inversely related: water contentwas low when temperature was high. The initial group, measured after the starving and

Table 3P. liÕidus. Mean values of MI and water content of the gonad in percent, all shown with the confidenceinterval value at 95%

Ž . Ž .Photoperiod Temperature 8C MI Water content %

Initial values 1.4"0.2 75.1"2.1LD 12 3.2"0.6 74.7"1.4LD 16 4.4"1.2 73.2"0.9LD 20 4.9"1.0 72.7"1.3LD 24 3.9"1.1 65.6"2.6SD 12 3.0"0.6 75.2"0.3SD 16 3.8"0.8 71.9"1.1SD 20 4.9"1.3 70.7"0.8SD 24 4.0"1.5 62.6"1.2


before the experiment, had about 75"2% water which was significantly higher than theŽ .values obtained after treatment except 128C . Although some relationship must exist

between the maturity stage and the water content of the gonads, this does not explain theunusual low moisture percentage obtained at 248C. This was much lower than the rangeobtained for wild individuals with all maturity stages pooled.

Ž . Ž .Concerning sexual maturity, no stage 6 fully mature or stage 8 post-spawned wereobserved, suggesting the individuals did not reach full maturation during the experiment.

Ž 2 .All treatments were significantly different from the initial one Watson U , Us0.225 ,Ž .meaning that every batch had gone forward in the reproductive process Fig. 5 . This

Ž .difference was marked by 1 gonads filled with reserve material, represented by a heavyŽ .network of nutritive phagocytes; and 2 the presence of some or many sexual cells.

ŽBasically, all sea urchins had reached a maturity stage, going from 3 to 5 recovering.stage, growing stage and premature stage, according to Spirlet et al., 1998a , all of

which are good for marketing. The echinoids were relatively in phase among thebatches: synchronicity in maturation is represented by the length of the vectors in Fig. 5Ž .i.e., homogeneity of the examined batch . Individuals matured faster as temperaturebecome higher except for the 248C treatment, where maturation speed was equivalent to

Fig. 5. P. liÕidus. Circular representation of the MI after polar transformation of the data. The vectorŽ . Ž .characteristics represent the mean value of the MI direction and the homogeneity of the values length . LD

and SD are long and short day, respectively. The numbers 12, 16, 20 and 24 are 8C temperature. Lines 1 to 8Ž .are the phases of soma and gonad development see Fig. 1 .


Ž 2 .that observed at 168C Watson U -test, Us0.225 . There was no significant differencebetween SD and LD photoperiod treatments, although maturation was faster at 128C and168C for the LD treatment.

4. Discussion

Populations of P. liÕidus in a land-based cultivation system lack the regular annualŽ .reproductive cycle that they have in the field Spirlet et al., 1998a . This phenomenon

Ž .has already been observed by Leahy et al. 1981 : initially, synchronous populations ofStrongylocentrotus purpuratus eventually drift apart in phase, within a period of 9 to 12months, when held in a maintenance system in the absence of seasonal environmentalstimuli. Different stages of the reproductive cycle are present at any one time, but there

Ž . Žis no well-defined spent phase empty gonads or growing phase gonads filling with. Ž .reserve material . Leahy et al. 1981 experimented with two possible ways to drive

Ž .asynchronous individuals into a phased condition: 1 spawn the echinoids repeatedly atŽ .1–2 months intervals until all late gametes are exhausted; 2 force a population of

females into a phased state where they are gravid and contain large reserves ofvitellogenic eggs by withholding spawning for one or two periods of 6 months or more.

Ž . ŽThese methods are too long. Knowing 1 that the gonads are storage organs see. Ž .Fernandez, 1996 for P. liÕidus notably , 2 that the individuals need to be sexually in

Ž . Ž .phase, 3 that the desired stage of the reproductive cycle is the growing stage, and 4that productivity implies the shortest delay possible, starvation seemed to be the mosteffective synchronizing method. Our study shows that after 2 months of starvation,

Ž . Žgonads are in the spent stage see Spirlet et al., 1998a , with a very low GI -2% in dry.weight . The virtual absence of mortality and the absence of care needed during

starvation make the method very attractive. After starvation, the gonads grow andmature in synchronicity, whatever the treatment.

ŽGonadal production is usually evaluated from the GI see Byrne, 1990; Lawrence etal., 1991; Urgorri et al., 1994; Guettaf and San Martin, 1995; Lozano et al., 1995;

.Fernandez, 1996 for P. liÕidus . Thus, gonadal growth cannot be dissociated fromsomatic growth. If two individuals produce the same mass of gonad and different masses

Ž .of soma, the one with the largest overall growth gonadal and somatic will present thelowest GI and will be regarded as less productive. With initial sexual synchrony, similarsize and GI, the differences in final GI express allocation of resources: the gonadsŽ . Ž . Žhigher GI or the soma lower GI . The gonad retrieval rate method calculated as the

.slope of the regression of gonad weight against total weight is another useful methodŽ .used by Byrne et al. 1998 . Nonetheless, the quality of the gonads is best described with

a combination of measures including GI, growth and MI. Variation of the water contentof the gonads appears to be a complementary indicator of gonad quality.

For P. liÕidus in land-based cultivation system, photoperiod has less influence thantemperature on the reproductive cycle and growth. Although, some effect was detectedon somatic growth, temperature seems to be the key factor in the metabolism andreproductive cycle of P. liÕidus in culture.

Ž .For a similar food intake, growth both soma and gonads is low at 168C andsubstantial at 248C. Thus, apart from its effect on metabolic rate, temperature seems to


affect the digestion efficiency andror the nutrient conversion process. This means that,Ž .in culture, the food conversion efficiency is low at low temperature. Klinger et al. 1986

showed for Lytechinus Õariegatus that for the same feeding rate, the sea urchin was lessŽefficient at processing food at 168C than at 238C. Several authors notably Lawrence et

.al., 1991 and Fernandez, 1996 for P. liÕidus have demonstrated the correlation betweengonadal growth, development and food intake.

Surprisingly, the most important growth was obtained with the 248C-SDs treatment,Ž .an unnatural condition. Ulbricht and Pritchard 1972 stated that intertidal species,

exposed to important temperature changes, present a ‘‘constant’’ metabolism whilesubtidal species, exposed to constant low temperature, are much more sensitive to

Ž .temperature variation. McBride et al. 1997 found gonadal production of S. francis-canus to be independent of temperature and explained that increased catabolism athigher temperature balanced the increase of food intake. Conversely, in our experiment,248C could possibly correspond to the peak of growth. Our results are in disagreement

Ž .with those of Le Gall et al. 1990 who found that the peak of somatic growth wasreached between 208C and 228C, and then decreasing abruptly until total mortality at298C.

In echinoids, photoperiod has been shown to influence mainly the gametogenic cycleŽ .McClintock and Watts, 1990; Pearse and Cameron, 1991 . This factor had never beentested as a potential somatic and gonadal growth enhancer, combined or not with otherfactors. Previous studies proved its ability to shift a seasonal gametogenic cycle in some

Ž . Žspecies Walker and Lesser, 1998 and thus to produce marketable gonads i.e., in the.growing or premature stages with a long-term exposure to inverted natural photoperiod.

In the present case, it does not have a significant influence on growth except at highŽ .temperature 248C . One must keep in mind that longer treatment might change this

conclusion.The fact that sea urchins generate soma and gonads separately is widely documented.

Resource allocation goes to maintenance, then to the digestive tract, a first stage inŽ .stocking nutrients Lawrence et al., 1991; Fernandez, 1996 , finally to the gonads, where

the nutrients accumulate in the scope of producing gametes and insure reproductionŽ .Pearse and Cameron, 1991 . At 128C, somatic production is negligible while some

Ž .gonads are produced. In only 45 days a relatively short time for echinoids , all batcheswith the exception of the low temperature treatment showed notable growth of bothsoma and gonads. The absence of intermediate measurements makes it impossible toknow if the compartments’ growth occurred successively or simultaneously. However,

Ž .the total somatic growth grossly between 10% and 25% per batch is substantial.Hence, it is reasonable to consider that somatic growth was progressive, along with the

Žgrowth of gonads, perhaps after a short period of recovery after starvation Bishop and. Ž .Watts, 1992 . The GI increase is also remarkable see Fig. 4 , especially when compared

to wild populations in Brittany, for which GI measurements in the field do not exceedŽ .8% see Spirlet et al., 1998a .

As previously mentioned, we have no indication that soma and gonads growseparately in time. The reason why a SD treatment gives better growth results is noteasily interpretable. Many field observations showed that echinoids in temperate climate

Žgrow more in the Winter Byrne, 1990; Turon et al., 1995; Fernandez, 1996 for P.´


.liÕidus , when the days are short. However, feeding is more important then and growthis proportionate. In our experiment, with equivalent amounts of food ingested, photope-riod had a direct effect on growth. To our knowledge, this has not yet been reported.

ŽTemperature had an important influence on the composition of the gonad water.content . Moreover, gonad water content decreased with increasing temperature. Conse-

quently, the SD-248C combination gave the best results in terms of growth, and also therichest gonads, in nutritional terms, as they contained only about 63% water. Thiscompares to the initial batch, which contained about 75% water, and to field specimens

Ž .for which the mean values were between 70% and 80% personal observation .Many studies have shown that temperature influences and regulates gametogenesis in

Ž .most echinoids living in temperate climate see Pearse and Cameron, 1991 for a review .Ž .In field populations, Spirlet et al. 1998a suggested that temperature acted as an

enhancer of the gametogenic process but probably not as a trigger signal. Thisobservation is confirmed here: the rate of gametogenesis increases with temperatureuntil it reaches 208C. In the Northern Atlantic coasts, as described by several authorsŽ .Byrne, 1990; Spirlet et al., 1998a , spawning takes place in late Spring and Summerwhen temperature reaches between 168C and 208C. This range must be optimal forfertilization and favourable for survival and development of the larvae. At 248C, weobserved fleshier but less mature gonads, meaning that high temperature can inhibit

Ž .andror interrupt the gametogenic process. Cochran and Engelmann 1975 have shownthat S. purpuratus loses the ability to spawn when temperature exceeds 178C and thatreproductive activity is turned off by elevated temperature. Gametogenesis in some other

Žechinoids Pseudocentrotus depressus, Yamamoto et al., 1988; Anthocidaris cras-.sispina and Hemicentrotus pulcherrimus, Sakairi et al. 1989 , is triggered by a drop in

temperature. It does not occur if the temperature is either constant or high. It would bereasonable to consider that high temperature represents a stress and is unfavourable forthe gametogenic process, and that the echinoids accumulate nutrients because these arenot converted into gametes.

Acknowledgements

We are grateful to J.M. Lawrence who supplied the artificial food. This research hasŽbeen supported by a EC research grant attributed to C. Spirlet ref. ERB 4001 GT92

. Ž0223 , in the framework of the Sea Urchin Cultivation contract no. AQ 2.530 BFE EC.‘‘FAR’’ Research Program . This paper is a contribution to the Centre Interuniversitaire

Ž .de Biologie Marine CIBIM .

References

Agatsuma, Y., Momma, H., 1988. Release of cultured seeds of the sea urchin Strongylocentrotus intermediusŽ .A. Agassiz , in the Pacific coastal waters of southern Hokkaido: I. Growth and reproductive cycle. Sci.Rep. Hokkaido Fish. Exp. Stn. 31, 15–25.

Bishop, C.D., Watts, S.A., 1992. Biochemical and morphometric study of growth in the stomach and intestineŽ .of the echinoid Lytechinus Õariegatus Echinodermata . Mar. Biol. 114, 459–467.


Byrne, M., 1990. Annual reproductive cycles of the commercial sea urchin Paracentrotus liÕidus from anexposed intertidal and a sheltered subtidal habitat on the west coast of Ireland. Mar. Biol. 104, 275–289.

Byrne, M., Andrew, N.L., Worthington, D.G., Brett, P.A., 1998. Reproduction in the diatematoid sea urchinCentrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia. Mar.Biol. 132, 305–318.

Cochran, R.C., Engelmann, F., 1975. Environmental regulation of the annual reproductive season ofŽ .Strongylocentrotus purpuratus Stimpson . Biol. Bull. 148, 393–401.

Conand, C., Sloan, N.A., 1989. World fisheries for echinoderms. Mar. Invertebr. Fish., 647–663.Fernandez, C., 1996. Croissance et nutrition de Paracentrotus liÕidus dans le cadre d’un projet aquacole avec

alimentation artificielle. These de doctorat, Universite de Corse, 278 pp.` ´Fernandez, C., Caltagirone, A., 1994. Growth rate of adult sea urchins Paracentrotus liÕidus in a lagoon

Ž .environment: the effect of different diet types. In: David, Guille, Feral, Roux Eds. , Echinoderms Through´Time. Balkema, Rotterdam, pp. 655–660.

Gomez, J.L.C., Tallon, J.G.M., Rodriguez, L.G.M., 1995. Experiments of sowing juveniles of ParacentrotusŽ . Ž .liÕidus Lamarck in the natural environment. In: Emson, Smith, Campbell Eds. , Echinoderm Research

1995. Balkema, Rotterdam, pp. 255–258.Grosjean, P., Spirlet, C., Gosselin, P., Vaitilingon, D., Jangoux, M., 1998. Land-based closed cycle

Ž .echiniculture of Paracentrotus liÕidus Lamarck Echinodermata: Echinoidea : a long term experiment at apilot scale. J. Shellfish Res. 17, 1523–1531.

Grosjean, P., Spirlet, C., Jangoux, M., 1996. Experimental study of growth in the echinoid ParacentrotusŽ . Ž .liÕidus Lamarck, 1816 Echinodermata . J. Exp. Mar. Biol. Ecol. 201, 173–184.

Grosjean, P., Spirlet, C., Jangoux, M., 1999. Comparison of three body-size measurements for echinoids. In:Ž .Candia Carnevali, M.D., Bonasoro, F. Eds. , Proceedings of the 5th European Echinoderm Conference.

Balkema, Rotterdam, pp. 31–35.Guettaf, M., San Martin, G.A., 1995. Etude de la variabilite de l’indice gonadique de l’oursin comestible´

Ž .Paracentrotus liÕidus Echinodermata: Echinoidea en Mediterranee nord-occidentale. Vie Milieu 45,´ ´129–137.

Jangoux, M., Larsonneur, C., Catoira Gomez, M., 1996. Sea urchin cultivation, final report of contract no. AQ2.530 BFE. FAR research program of the ECC, 96 pp.

Kelly, M.S., McKenzie, J.D., Brodie, C.C., 1998. Sea urchins in polyculture: the way to enhanced gonadŽ .growth?. In: Mooi, R., Telford, M. Eds. , Echinoderms: San Francisco. Balkema, Rotterdam, pp.

707–711.Klinger, T.S., Hsieh, H.L., Pangallo, R.A., Chen, C.P., Lawrence, J.M., 1986. The effect of temperature on

feeding, digestion, and absorption of Lytechinus Õariegatus. Physiol. Zool. 59, 332–336.Klinger, T.S., Lawrence, J.M., Lawrence, A.L., 1998. Digestion, absorption and assimilation of prepared feeds

Ž .by echinoids. In: Mooi, R., Telford, M. Eds. , Echinoderms: San Francisco. Balkema, Rotterdam, pp.713–721.

Ž .Lawrence, J.M., 1985. The energetic echinoderm. In: Keegan, B.F., O’Connor, B.D.S. Eds. , Echinodermata.Balkema, Rotterdam, pp. 47–67.

Lawrence, J.M., Fenaux, L., Corre, M.C., Lawrence, A., 1991. The effect of quantity and quality of preparedŽ .diets on production in Paracentrotus liÕidus Echinodermata: Echinoidea . In: Scalera-Liaci, L., Canicatti,

Ž .C. Eds. , Echinoderm Research. Balkema, Rotterdam, pp. 107–110.Leahy, P.S., Hough-Evans, B.R., Britten, R.J., Davidson, E.H., 1981. Synchrony of oogenesis in laboratory

Ž .maintained and wild populations of the purple sea urchin Strongylocentrotus purpuratus . J. Exp. Zool.215, 7–22.

Ž .Le Gall, P., 1990. Culture of echinoderms. In: Barnabe, G. Ed. , Aquaculture 1 Ellis Horwood, New York,pp. 443–462.

Le Gall, P., Bucaille, D., 1989. Sea urchins production by inland farming. In: De Pauw, N., Jaspers, E.,Ž .Ackerfors, H., Wilkins, N. Eds. , Aquaculture — a biotechnology in progress. European Aquaculture

Society, Breden, Belgium, pp. 53–59.Le Gall, P., Bucaille, D., Grassin, J.B., 1990. Influence de la temperature sur la croissance de deux oursins´

comestibles Paracentrotus liÕidus et Psammechinus granularis. In: De Ridder, C., Dubois, P., Lahaye,Ž .M.C., Jangoux, M. Eds. , Echinoderm Research. Balkema, Rotterdam, pp. 183–187.

Lozano, J., Galera, J., Lopez, S., Turon, X., Palacin, C., Morera, G., 1995. Biological cycles and recruitment


Ž .of Paracentrotus liÕidus Echinodermata: Echinoidea in two contrasting habitats. Mar. Biol. Prog. Ser.122, 179–191.

McBride, S.C., Pinnix, W.D., Lawrence, J.M., Lawrence, A.L., Mulligan, T.M., 1997. The effect oftemperature on production of gonads by the sea urchin Strongylocentrotus franciscanus fed natural andprepared diets. J. World Aquacult. Soc. 28, 357–365.

McClintock, J.B., Watts, S.A., 1990. The effects of photoperiod on gametogenesis in the tropical sea urchinŽ . Ž .Eudaris tribuloides Lamarck Echinodermata: Echinoidea . J. Exp. Mar. Biol. Ecol. 139, 175–184.

Pearse, J.S., Cameron, R.A., 1991. Echinodermata: Echinoidea. In: Reproduction of marine invertebrates.Ž .Giese, A.C., Pearse, J.S., Pearse, V.B. Eds. , Echinoderms and Lophophorates VI Boxwood Press, pp.

513–662.Pearse, J.S., Pearse, V.B., Davis, K.K., 1986. Photoperiodic regulation of gametogenesis and growth in the sea

urchin Strongylocentrotus purpuratus. J. Exp. Zool. 237, 107–118.Robinson, S.M.C., Colborne, L., 1998. Roe enhancement trials of the green sea urchin using an artificial food

Ž .source. In: Mooi, R., Telford, M. Eds. , Echinoderms: San Francisco. Balkema, Rotterdam, p. 803.Sakairi, K., Yamamoto, M., Ohtsu, K., Yoshida, M., 1989. Environmental control of gonadal maturation in

laboratory reared sea urchins: Anthocidaris crassispina and Hemicentrotus pulcherrimus. Zool. Sci. 6,721–730.

Spirlet, C., Grosjean, P., Jangoux, M., 1998a. Reproductive cycle of the echinoid Paracentrotus liÕidus:analysis by means of the maturity index. Invertebr. Reprod. Dev. 34, 69–81.

Spirlet, C., Grosjean, P., Jangoux, M., 1998b. Optimizing food distribution in closed-circuit cultivation ofŽ .edible sea-urchins Paracentrotus liÕidus: Echinoidea . Aquat. Living Resour. 11, 273–277.

Turon, X., Giribet, G., Lopez, S., Palacin, C., 1995. Growth and population structure of Paracentrotus liÕidus´Ž .Echinodermata: Echinoidea in two contrasting habitats. Mar. Ecol. Prog. Ser. 122, 193–204.

Ulbricht, R.J., Pritchard, A.W., 1972. Effect of temperature on the metabolic rate of sea urchin. Biol. Bull.Ž .Mar. Biol. Lab. Woods Hole 142, 178–185.

Urgorri, V., Reborada, P., Troncoso, J.S., 1994. Dispersion, demografia y produccion gonadal de una´ ´Ž .poblacion de Paracentrotus liÕidus Lamarck, 1816 . Memoria final de resultados del P.I. FEUGA,´

University Santiago de Compostela.Walker, C.W., Lesser, M.P., 1998. Manipulation of food and photoperiod promotes out-of-season gametogene-

sis in the green sea urchin Strongylocentrotus droebachiensis: implication for aquaculture. Mar. Biol. 132,663–676.

Yamamoto, M., Ishine, M., Yoshida, M., 1988. Gonadal maturation independent of photic conditions inlaboratory reared sea urchins, Pseudocentrotus depressus and Hemicentrotus pulcherrimus. Zool. Sci. 5,979–988.

Zar, J.H., 1996. Biostatistical analysis. 3rd. edn. Prentice-Hall.

urchins, paracentrotus li idus / lamarck / echinodermatadirectory.umm.ac.id/data...

Documents