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Journal of Experimental Marine Biology and Ecology 245 (2000) 183–196

www.elsevier.nl / locate / jembe

The effect of feeding or starvation on resource allocation to

body components during the reproductive cycle of the sea

urchin Sphaerechinus granularis (Lamarck)

a ,_* b c

Monique Guillou , Lawrence J.L. Lumingas , Christine Michel

´ ´

UMR CNRS6539, Universite de Bretagne Occidentale, Institut Universitaire Europeen de la Mer,

´ Place Nicolas Copernic, 29280 Plouzane, France

Department of Marine Science and Technology, Faculty of Fisheries, Sam Ratulangi University,

Kampus Unsrat-Bahu, 95115 Manado, Indonesia

Station de Biologie Marine du Museum National d’Histoire Naturelle et du College de France,

Place de la Croix, BP 225, F29182 Concarneau, France

Received 23 July 1999; received in revised form 9 October 1999; accepted 20 October 1999

Abstract

To determine the effects of feeding or starvation on resource allocation to body components during the reproductive cycle of Sphaerechinus granularis, sea urchins were placed in laboratory tanks and either fed ad libitum or starved during two different periods of their biological cycle, i.e. the mature stage and the recovery stage. The urchin growth was monitored over the whole experimental period, the gonad, gut, lantern indices and organic matter levels of different organs were determined at the end of the experiment. During the mature stage sea urchins in good nutritional conditions did not increase in size, but allotted energy to gonad production and stored reserves in body wall. Limiting food stopped the gonadal growth without complete regression. During the recovery period food allowed somatic growth, i.e. test growth and the storage of reserves in gonad somatic cells. This somatic production did not occur under food-limited conditions and the resources allotted for survival and maintenance were taken from different body components.  2000 Elsevier Science B.V. All rights reserved.

Keywords: Food supply; Gonad development; Growth; Resource allocation; Sea-urchin

*Corresponding author. Tel.: 133-02-9849-8634; fax: 133-02-9849-8645.

E-mail address: [email protected] (M. Guillou)

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1. Introduction

Numerous field and laboratory studies conducted on echinoderms have led to the conclusion that any variation in food supply highly influences the allocation of resources to somatic and gonadal growth function. Food quality and quantity both affect sea urchin growth (reviewed by Lawrence and Lane, 1982). Food limitation slows down growth rate, and can lead to re-absorption of material from the body wall and a reduction in test

diameter (Ebert, 1967, 1968; Dix, 1972; Regis, 1979; Levitan, 1988, 1989, 1991). Different components of somatic growth may also vary like, for example, Aristotle’s lantern which by lower nutrient conditions becomes bigger and larger compared to the overall body size (reviewed by Ebert, 1996). Sometimes, gametogenesis and maturation are also affected under poor nutritional conditions, and may be arrested (reviewed first by Lawrence and Lane, 1982 then, by Xu and Barker, 1990 for asteroids, and Minor and Scheibling, 1997 and Russell, 1998 for strongylocentrotid sea urchins). But most of the authors have not considered the effect of the reproductive state on the expression of the observed responses; indeed, it is likely that variations in food ration affect energy partitioning in a way which depends on the reproductive state. As little information is available on this subject, several questions remain: (i) During the gonad maturation of sea urchins can a larger ration of food increase the somatic growth rate usually reduced during this stage of biological cycle (reviewed by Guillou and Michel, 1994)? (ii) Can it produce gonadal growth in the post-spawning phase, i.e. a build up of storage reserves? (iii) Lastly, how will starvation act on somatic and gonadal growth over these different reproductive periods?

In an attempt to answer to these questions, and with the aim of understanding the patterns of energy allocation to growth and reproduction functions over an annual cycle, several laboratory experiments were conducted on fed and starved urchins before and after their spawning period. The sea urchin, Sphaerechinus granularis, was chosen because of its large number in the Glenan Archipelago (Southern Brittany, France) and of previous studies dealing with its reproductive cycle in Brittany. Its annual cycle of gonadal growth is characterised by a short breeding season in spring, usually within the end of March and May, which depends on the seawater temperature during the gonadal growth before spawning (Guillou and Michel, 1993). This brief breeding season is followed by a fast post-spawning recovery concomitant with the development of nutritive tissue in the gonads (Guillou and Lumingas, 1998). A long mature stage extends from autumn to early spring with a possible decrease in gonad index attributed to the use of reserves whenever seawater temperature is abnormally low. The comparisons of various populations of this species living in different areas (Mortensen, 1943; Keckes in Fenaux, 1972; Semroud and Senoussi, 1989; Soualili, 1998) have shown that environmental conditions such as food supply and the ‘energy reserves to generate mature gametes’ (Cochran and Engelmann, 1975) highly control the gonad volume whereas seawater temperature acts more on the reproductive cycle chronology than on the fecundity rate (Guillou and Michel, 1993; Guillou and Lumingas, 1998). A better understanding of nutrient use and allocation to different body components over the reproductive cycle could lead to ways of increasing the somatic and gonadal growth of this potential aquaculture species.

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2. Materials and methods

Sphaerechinus granularis individuals were collected in the Glenan Archipelago in 1991, 1992 and 1993 at two different seasons corresponding to two stages of their reproductive cycle. The first group was sampled during the maturation stage, at the end of January or early February, when the period of possible winter gonad decreases had ended (Guillou and Lumingas, 1998). The second group was collected in mid July after the breeding season. These sea urchins were transferred to the Marine Laboratory of Concarneau. In February and July 1991 only 40 urchins whose size ranged within 85 and 100 mm were kept for experimental use whereas in 1992 and 1993 the method was improved by both selecting 80 urchins and reducing the size interval to 85–95 mm to minimise the variation in organ indices between individual urchins. The collection of samples ended in January 1993.

The urchins were randomly placed in four glass tanks (82337338 cm) each of them containing the same number of individuals, i.e. ten in 1991, 20 in 1992 and 1993 respectively. The tanks were filled with fresh running seawater at a temperature ranged from 7 to 98C in winter to 18–198C in summer (Fig. 1) close to that found in the natural environment. There were two replicates of each treatment, the ‘fed 1’ and ‘fed 2’ replicates were fed every 4 d on freshly collected Laminaria digitata (Hudson) Lamouroux, their preferred algae (Guillou and Michel, pers. obs) which was supplied always in excess. Each time they were fed, the tanks were cleaned, and on the basis of

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the previous study of Guillou and Michel (1994), about 500 mg DW d ind of Laminaria were introduced into them, but no measurement was done to control the amount of food ingested. The ‘starved 1’ and ‘starved 2’ replicates were not fed at all. In 1992 and 1993 the experiment carried out on individuals in the gonadal growth stage (sampled in January–February) ended in April as soon as spawning was observed in the natural environment where the reproductive condition of the sea urchins was monitored monthly. This experiment was denoted ‘Maturity period’. In 1991 growth measurements were carried out until the end of June. For the urchins sampled after spawning (mid-July), the experiment was stopped at the end of October 1991 and of September in 1992 and was denoted ‘Recovery period’ (Fig. 2).

In order to investigate the effects of food supply on energy allocation during these two stages of the reproductive cycle, three set of parameters were determined: (i) the changes

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Fig. 2. Schematic diagram showing the temporal changes in the gonad indices of Sphaerechinus granularis in the Glenan Archipelago with location of the maturity (M) and recovery (R) periods and indication of the list of parameters analysed during these two stages in 1991, 1992 and 1993.

in the diameter of the tests and wet weights of the urchins over the experimental period were recorded, (ii) gonad-, gut- and lantern-indices were measured at the end of experiment, and (iii) the percentage of organic matter (OM) contained in the different organs was determined at the end of experiment (Fig. 2). For both the 1992-recovery period and 1993-maturity period, the three organ indices were estimated on 30 urchins of the same size collected by diving in the sampling site, the Glenan Archipelago, before (pre) and after (post) laboratory experiments. Before these experiments the OM percentage in the different organs of these urchins was also determined. Only growth measurements were made during the ‘1991 maturity period’. All urchins were measured and weighed at the beginning of each experiment, then approximately every 2 weeks over the experimental period. Horizontal test-diameter was measured along two perpendicular axes (0.5-mm accuracy). The mean diameter was used for comparisons.

Total body wet weight was measured (10 g accuracy) once superficial water had been drained on filter paper. At the end of experiment all the urchins were dissected, then their gonads, emptied guts, Aristotle’s lanterns and tests were dried to constant weight at 608C. The gonad-, gut- and lantern-indices were calculated as the dried organ to eviscerated test dry weight ratio multiplied by 100. The percentages of organic matter in body wall, gonads, guts, lanterns and peristomial membranes were deduced from ash values weighted once tissues had stayed in a muffle furnace at 4508C for 4 h.

To estimate the size and weight increase over the whole experiment, the mean size and weight were regularly calculated per tank (at the time of each measurement as

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indicated above), then compared. There were four to seven measurements per experi-ment depending on the measureexperi-ment periodicity. One-factor ANOVA (P,0.05) with the LSD test was applied to compare the data, i.e. mean sizes and weights, various indices and the percentages of organic matter per components, once homogeneity of variances had been tested. All analyses were performed with the statistical software STATGRAPHICS.

3. Results

3.1. Growth

The comparison of sea urchin growth between the two reproductive periods showed that sea urchin response to variation in food supply depended on their sexual state. As no significant differences in the initial starting weight and diameter were found between

Fig. 3. Changes in mean test diameter and wet weight (6S.D.) for starvedxand fed♦urchins during the maturity period.

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replicates of the same treatments and because the growth pattern of these replicates was similar, Figs. 3 and 4 illustrates pooled replicates.

3.1.1. Maturity period

The test diameter and wet weight of Sphaerechinus granularis (Fig. 3) did not change significantly (P.0.05) in fed and starved urchins during the three years, except between February and April 1992 when a low but significant increase (P,0.05) in the test diameter of fed urchins was observed but without any significant variation in wet weight. 3.1.2. Recovery period

The response of fed urchins (Fig. 4) differed greatly from that observed with the starved ones. The test diameter and wet weight of starved individuals did not vary significantly (P.0.05) while in the fed urchins the final values for both test diameters and wet weights were always significantly higher than the initial ones. The test diameter of fed urchins gradually increased by 4–6 mm and the wet weight by 24–43 g. 3.2. Indices

Because there were no significant differences among replicates within treatments, the data were presented as pooled replicates in Fig. 5.

3.2.1. Gonad indices (GI)

At the end of the two annual experiments, the mean gonad indices of fed urchins were significantly higher than those of starved ones over both the recovery and the maturity

Fig. 4. Changes in mean (6S.D.) test diameter and wet weight for starvedxand fed♦urchins during the recovery period.

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Fig. 5. Comparison of mean (6S.D.) gonad (GI), gut (GtI) and lantern indices (LI) at the end of the recovery (1991; 1992) and maturity periods (1992; 1993) in laboratory experiment (starved, st, and fed urchins, fd) and in the natural environment before (pr) and after (post) the laboratory experiment (92 for the 1992 recovery period; 93 for the 1993 maturity period).

phases (Fig. 5). The 1992 experiment showed that at the end of the recovery period (i) the starved urchins presented a GI significantly lower (P,0.05) than the preexperimen-tal value (termed ‘pr 92’ on Fig. 5), (ii) the GI of fed urchins were significantly higher than the value measured concomitantly in the population in the natural environment (termed ‘post 92’ on Fig. 5). At the end of the maturity period (i) the GI of starved urchins did not significantly differ from the preexperimental value, (ii) the GI of fed urchins did not significantly differ from the value measured at the same time in the reference population in the natural environment (post 92). At the end of the maturity period, over the two gonadal cycles studied the GI of starved urchins were significantly higher (P,0.05) than at the end of the recovery period (e.g.: st-mat92.st-rec91 and st-mat93.st-rec92 where st represents the starved urchins, mat the maturity period and rec the recovery period). This increase could be interpreted as evidence of gameto-genesis despite starvation.

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3.2.2. Gut indices (GtI)

The analysis of gut index results did not display any obvious pattern. At the end of the 1991-recovery period and 1992-maturity period the gut index of fed urchins was significantly higher than that of the starved ones (P,0.05); these differences were not significant in the two other experiments (1992-recovery period and 1993-maturity period). The 1992 and 1993 experiments did not reveal differences (P.0.05) between the preexperimental value and GtI the of starved and fed urchins except for the starved urchins of the 1993-maturity period that had significantly higher GtI. At the end of the 1992-recovery period, the GtI of the population in the natural environment was significantly higher (P,0.05) than that of the laboratory starved and fed urchins. 3.2.3. Lantern indices (LI)

No difference in the lantern indices was observed between the treatments (P.0.05) except at the end of the 1992-recovery period when the lantern indices of fed urchins were significantly lower than those of the starved ones and than the preexperimental value. At this time the LI of the population in the natural environment was significantly the lowest.

3.3. Level in organic matter

As there were no significant differences between replicates within treatments, Fig. 6 illustrates pooled fed (f) and starved (st) groups.

3.3.1. Test

At the end of the two annual experiments, the levels of organic matter (OM) in the test of fed urchins were significantly higher (P,0.05) than those of starved ones over both the recovery and the maturity phases. At the end of the 1992-recovery period, the pre-experimental (pr92) OM level was significantly higher than OM level in the starved urchins, but did not differ from that of the fed urchins. At the end of the 1993-maturity period no significant difference (P.0.05) was observed between the fed and starved urchins. However the OM level of fed urchins was significant higher than the pre-experimental value (pr93).

3.3.2. Gonads and gut

At the end of the recovery period the OM pattern in these two organs was the same as in the test with OM levels significantly lower (P,0.05) in the starved urchins than in the fed ones and than the 1992-pre-experimental value. Contrary to the test, OM levels did not significantly differ in fed and starved urchins at the end of the maturity period (P.0.05). The only difference between gonads and gut was that OM levels in the gut of starved and fed urchins were higher (P,0.05) than the preexperimental value while they did not significantly differ in the gonads (P.0.05).

3.3.3. Lantern and peristomial membranes

At the end of the 1992-recovery period, the OM level in fed urchins was significantly higher than the one in starved urchins although this was not the case in 1991. The 1992

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Fig. 6. Comparison of mean (6S.D.) organic matter level (%) in the different organs (test, gonads, gut, lantern and peristomial membranes) at the start of the laboratory experiment (pr) (92 for the 1992 recovery period; 93 data for the 1993 maturity period) and at the end of the laboratory experiment (starved, st, and fed urchins, f).

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OM levels in fed and starved urchins were significantly lower than the pre-experimental value (P,0.05). At the end of the 1993-maturity period, no significant difference (P.0.05) was observed between the OM levels (preexperimental, fed and starved urchins).

To summarise (i) at the end of the recovery period, the OM levels in test, gonads and gut of fed urchins were always significantly higher than those of the starved groups, as were the OM values in lantern and in peristomial membranes over 1992 treatments. The pre-experimental value was significantly higher than all the OM levels recorded in 1992 starved urchins. It did not differ from the OM levels of fed urchins except in lantern and peristomial membranes where the OM was significantly reduced (ii) at the end of the maturity period, no significant differences were observed in the gonads, guts and peristomial membranes between starved and fed urchins. The OM levels in the test, gonads and lantern of starved urchins did not differ from the pre-experimental values, whereas they were increased in the test and gut of fed urchins. Consequently, throughout the recovery period the starved urchins were obviously losing organic matter from the test (body wall) and gonads. On the other hand, the fed urchins stored organic matter in their body wall over the maturity period.

4. Discussion

The previous studies on Sphaerechinus granularis in Brittany carried out by Guillou and Michel (1993, 1994) showed the seasonal changes observed in their somatic and gonadal growth which could be to split into two stages: the pre and post spawning. Three or four months before the spawning (maturity period), there is no variation in weight and test diameter while GI is increasing; this implies an allocation of energy to only gonadal growth. Post spawning, there is a short rest period (August), then the recovery period starts over the autumn, and energy is allocated to both somatic (body wall increase) and gonadal growth. The study reported here provides additional and significant information on the effects of feeding and starvation on energy allocation during these two reproductive stages.

The experimental results showed that high food availability changed the pattern of gonadal and somatic growth of Sphaerechinus granularis; these changes were much more noticeable over the recovery period than over the maturity stage. During the maturity period, while GI increased in a pattern similar to that of the natural environment, neither the test diameter nor the weight increased. However the changes in organic matter levels indicated that excess of food was converted into nutrient reserves in the test and gut. During the recovery period, test growth rate and gonad indices were higher than those observed in the natural environment, but without reserve storage in the test and gut.

When the sea urchins were starved, they showed during the maturity period neither gonadal growth, nor test growth as for the fed treatment, nor significant diameter decrease as pointed out by several authors after prolonged starvation (Ebert, 1967, 1968;

Dix, 1972; Regis, 1979; Levitan, 1988, 1989, 1991). However, the gonads did not totally regress. No decrease in the organic matter level in the test was observed. During the

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recovery period, the sea urchins showed neither somatic growth nor gonadal growth. The gonad indices were minimal. The organic matter level significantly decreased in all the body components, especially in the test and gonads. A lantern index higher in starved urchins than in well-fed urchins was noticed. However, this difference should be attributed more to the diameter increase of well-fed sea urchins (observed over the recovery period) than to the growth of the Aristotle’s lantern of the food-limited individuals.

The lack of test growth during the maturity stage although the urchins were fed to excess suggests somatic growth may be influenced by factors other than food availability, e. g. temperature. It has been shown that a winter decrease in sea water temperature slows down growth rate by decreasing food consumption and assimilation (Lawrence, 1975; Klinger et al., 1986; Lares and McClintock, 1991). Our experimental treatments were thus partly biased due to environmental factors interactions. However, the decrease in the amount of algae introduced in the tanks (Guillou and Michel, pers. obs.) and the difference observed in gonadal growth trend according to the diet experiments highlight that low temperature did not stop food consumption during the maturity stage. Another factor influencing somatic growth may be the food quality. In this study we considered the energy allocation pattern in Sphaerechinus granularis only fed algal diets. Many recent studies have been carried out to evaluate the effect of manufactured feeds on sea urchin somatic and gonadal growth within the scope (development) of aquacultural practice. Most of them confirms the present conclusions. They indeed indicated that diet containing animal-derived proteins and lipids does not significantly increase somatic growth during the pre-spawning period of Paracentrotus lividus (Fernandez and Galtagirone, 1994), of Strongylocentrotus droebachiensis (Klinger et al., 1997; Walker and Lesser, 1998) or Evechinus chloroticus (Barker et al., 1998). Cook et al. (1998) suggested, however, that a high energetic animal food can, all over the year, support and enhance both somatic and gonadal growth in Psammechinus miliaris. An important energetic diet may sometimes highly modify the sea urchin energy allocation pattern. Each species, however, must be considered independently according to its natural diet. In the present case P. miliaris is certainly more carnivorous (Hancock, 1957) than S. granularis (Cornet and Jangoux, 1974) and the response of these urchins can thus vary with the food quality.

In conclusion, over the maturity period, Sphaerechinus granularis somatic growth does not take place. Sea urchins in good nutritional conditions allocate energy to gonad production and may store reserves in body wall without growing. When food becomes limiting, gonadal growth is stopped without necessarily total regression. A slight reproductive activity could thus remain. A previous study from two natural populations of the same species and of the same size had shown that food-limited sea urchins always displayed lower repletion and gonad indices (Guillou and Lumingas, 1999). During the recovery period, when food is available, gonadal and somatic growth occurs, reserves are only accumulated in gonads, inside the somatic-cells (Guillou and Lumingas, 1998). The accumulation of reserves in this organ appears preponderant and, over a short time, it could forbid nutrient storage inside the body wall and gut; this conclusion was also drawn by Russell (1998). Under food-limited conditions gonadal and somatic growth does not restart and the resources used for survival and maintenance are mainly taken

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from the body wall and gonads if the gonadal growth has already started. This use of reserves from storage organs is not observed throughout the maturity period. It has been shown that under nutritional stress conditions organic matter is taken from the body wall (Ebert, 1996; Lares and Pomory, 1998) and from the gonads (lipids) (Fenaux et al., 1977; Lawrence and Byrne, 1994). As no decrease of the test diameter was noticed in the study reported here, it is likely that starvation does not lead to calcite resorption as previously shown in other sea urchins, unless the length of experimentation was too short to cause this loss.

This preliminary study showed response variability in term of energy allocation according to the reproductive state. It also suggested that during the maturity period in the natural environment, some processes controlling energy allocation are not influenced by the direct environmental conditions. This ecological approach should be completed by further investigations on the intrinsic factors regulating reserve partitioning, especial-ly the sexual hormones whose levels in reproductive and somatic organs fluctuate with reproductive and nutritional states.

Acknowledgements

We are grateful to Mr. Y. Le Gal., Director of the Marine Station of Concarneau (France), for the use of the MV ‘Garvel’ and laboratory facilities and R. Marc for assistance in the field. We also thank Pr J.M. Lawrence for valuable discussions about this theme of research and M.P. Friocourt for help in the writing of English manuscript and useful criticism. [SS]

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