Energetic requirements during Gonad maturation and spawning in scallops: sex differences in Chlamys islandica (Muller 1776).

ABSTRACT Reproduction in scallops, as in many broadcast-spawning invertebrates, involves the production of a gonad that can become the largest tissue in the body. Gonad maturation leads to mobilization of macmmolecular reserves from somatic tissues in many scallops. Because ovaries typically contain higher energetic contents than testes, we examined whether the energetic investment in gonad production and spawning and the impact on somatic tissues was greater in temale than male Iceland scallops, Chlamys islandica. In males and females, maturation led to accumulation of carbohydrate and protein in the gonads, whereas lipids only accumulated in the ovary. In both sexes, the increase in gonad mass was accompanied by decrease of carbohydrate in muscle and the remaining tissues. but testes maturation was also paralleled by loss of carbohydrates and lipids from the digestive gland. Although spawning led to a greater energy loss in the female than in the male gonads (73 vs. 49 kJ in gonad energy content), less mobilization of somatic energy was observed during gametogenesis and spawning in females than males (14.5 kJ vs. 36.7). Most of the energy requirements for maturation and spawning in females must have been covered by feeding, whereas somatic reserve mobilization could have covered most of these costs in males. As in most scallop species, lipids account for a major part of the ovarian energy content. Direct deposition of dietary lipids in the eggs could minimize the impact on somatic tissues of female scallops. The costs of protein synthesis during testes maturation could decrease the aerobic scope available for feeding by males. In light of our previous demonstration of the impact of gonad maturation in C. islandica on recuperation from exhaustive exercise, our results suggest that the survival of males may be decreased more by their reproductive investment than that of females. The bioenergetic strategies of female scallops seem to favor survival and hence future reproduction more than those of male scallops.

KEY WORDS: biochemical reserves, Chlamys islandica, reproduction, reproductive cost, scallops, sex differences

INTRODUCTION

Intraspecific variation in how the reproductive cycle of scallops affects the mass and biochemical composition of body components has been attributed to the timing of gonad proliferation (Shafee 1981), to the habitat of the populations under study (eg. depth, protected or exposed) (MacDonald & Thompson 1986, Bricelj et al. 1987, and Epp et al. 1988), to the size or age group examined (Epp et al. 1988 and Martinez 1991), to the abundance and quality of the food supply, and to temperature (Shafee 1981, MacDonald & Thompson 1986, and Martinez et al. 2000). However, little is known about differences in reproductive investment between male and female scallops. In hermaphroditic scallops, the question of the relative investment in the male and female portion of the gonad is intriguing (Faveris & Lubet 1991), but marked qualitative and quantitative differences in reproductive investment of males and females are likely in species in which sexes are separate.

The cost of reproduction is typically believed to be higher in females than in males, given the large size of the egg relative to the sperm. Nuptial gifts, territorial defense, and paternal care of offspring can make the cost of reproduction higher for males than females. However, in broadcast spawning scallops, such behavioral considerations are unlikely to modify the cost of reproduction. The tact that the gonad can be the largest organ in scallops clearly indicates high investment in reproduction (Barber & Blake 1991), but whether the impact of this investment varies between males and females is an open question. The little that is published about sex differences in reproductive investment indicates that male and female scallops can differ in the size of the gonad (Couturier & Newkirk 1991) and although the mature ovary and testis have similar protein contents, the ovary is richer in lipid (Couturier & Newkirk 1991 and Brokordt et al. 2000a). Various studies have examined reproductive investment in scallops, but most present pooled data for males and females. If investment in a given reproductive cycle decreases individual survival, it would reduce future reproductive success and thereby decrease fitness. Thus, reproductive investment represents a compromise between current and future reproduction. These compromises will differ between males and females if their equations linking reproductive investment with reproductive success and individual survival differ.

Mobilization of somatic reserves in support of reproduction should vary as a function of reproductive investment and of food availability. Mobilization of glycogen from the adductor muscle in support of gametogenesis and spawning occurs even when food availability is high (see Barber & Blake 1991 for review). In the Iceland scallop, C. islandica, and in the tropical scallop, Euvola ziczac, glycogen mobilization during gonad growth is accompanied by decreases in muscle activities of enzymes in energy metabolism and in the capacity to recover from exhaustive exercise (Brokordt et al. 2000a and Brokordt et al. 2000b). In Argopecten purpuratus, the decrease of muscle glycogen during gonad maturation also coincided with a marked decrease in escape capacities (clapping and recovery, K. Brokordt, unpubl. data). This suggests that mobilization of somatic reserves in scallops may decrease individual survival during attack by predators. In the black scallop, Chlamys varia, gametogenesis and spawning occur during periods of high and low food availability (spring and autumn, respectively), and only the autumn reproduction leads to extensive mobilization of protein, lipid, and carbohydrate from somatic tissues (Shafee 1981). In a comparison of two successive reproductive cycles in E. ziczac, recuperation from exhaustion was more impaired in the first cycle in which reproductive investment was high while food availability was low. Muscle protein levels only declined during the first cycle, whereas muscle glycogen and enzyme levels declined during both cycles (Brokordt et al. 2000b). In these scallop species, gametogenesis and spawning consistently lead to depletion of muscle glycogen, but their impact on other somatic reserves and recuperation from exhaustion (in the case of E. ziczac) varies according to food availability and the extent of reproductive investment.

In this study we examined whether male and female Iceland scallops, C. islandica, differ in their reproductive investment and somatic reserve mobilization during a reproductive cycle. The greater lipid levels in mature ovaries (Brokordt et al. 2000a) suggest that females invest more energy in reproduction than males. However, as the synthesis of lipids may be less costly than that of proteins, the cost of spermatogenesis may exceed that of ovogenesis. In the northern Gulf of St. Lawrence, a natural population of C. islandica shows marked and rapid gonad maturation during the spring increase in phytoplankton followed by a precipitous and synchronous spawning (Arsenault & Himmelman 1998). We sampled sexually mature males and females in a narrow size range (shell height = 79-81 mm) while their gonads were immature (May 30), mature (July 20) and after spawning (August 14). The mass and biochemical composition of the body components were measured and converted to energetic units using calorific coefficients to assess whether males and females differed in their reproductive investment and in its impact on somatic reserves. We measured carbohydrate, protein and lipid levels in the gonads, digestive gland, remaining tissues, (mantle, gill, foot, etc) and protein and glycogen levels in the adductor muscle. Because lipid levels in the adductor muscle are below 5% of dry mass (Couturier & Newkirk 1991) and typically change little throughout the reproductive cycle, they were not measured.

MATERIALS AND METHODS

Sampling, Animals, and Tissue Analyses

We studied the population of Chlamys islandica in the Mingan Islands (50[degrees]14'N, 63[degrees]36'W) in the northern Gulf of St. Lawrence, eastern Canada. Adult scallops (height 79-81 mm), 15 females and 15 males, were collected by SCUBA diving at 37 m in depth on May 30. July 20, and August 14, 2000. For both females and males, these sampling dates corresponded to when the gonads were immature, completely mature, and spawned. At each sampling period, we determined the shell height and wet and dry masses (oven-dried for 48 h at 80[degrees]C) of four body components: gonad, muscle, digestive gland, and the remaining tissues (mantle tissue, gills, excretory organ, foot, etc., henceforth referred to as remaining tissues). Tissues were frozen at -20[degrees]C, transported frozen to Universite Laval, and then stored at -70[degrees]C until biochemical analysis.

Biochemical and Energetic Analyses

We determined the carbohydrate content in the female and male gonads, digestive gland, and remaining tissues using the phenol-sulfuric acid method of Dubois et al. (1956), as modified by Martinez (1991), with mussel glycogen as the standard. For the adductor muscle we determined the glycogen content by enzymatic hydrolysis with amyloglucosidase as described by Keppler and Decker (1974). The protein content in gonads, muscle, digestive gland, and remaining tissues was determined using the bicinchoninic acid method of Smith et al. (1985), with bovine serum albumin as the standard. We determined the lipid content of all tissues (except for muscle) by extraction with chloroform-methanol according to Folch et al. (1957) and colorimetric determination with phosphovanillin, using tripalmitin as the standard (Postma & Stroes 1968).

Energy losses and gains by each body component during gonad maturation and spawning were estimated using the following energy conversion factors: carbohydrate = 17.2 kJ [g.sup.-1] protein = 20.1 kJ [g.sup.-1], lipid = 35.3 kJ [g.sup.-1] (Brody 1945 and Beukema & De Bruin 1979). These factors were applied to mean values of each biochemical component measured during the reproductive cycle.

We present the tissue mass and biochemical components on a per animal basis, (ie, as absolute composition). This was possible as we sampled animals over a narrow size range. Other forms of presentation may confound interpretation of results (Couturier & Newkirk 1991) (ie, relative composition involves reciprocal relationships between the components and this may lead to misinterpretation of the underlying biologic phenomena).

Statistical Analyses

For all comparisons between sampling dates for each sex we analyzed the data using one-way ANOVAs to test the null hypotheses of no differences between reproductive stages (Sokal & Rohlf 1981), Comparisons between sexes at specific sampling dates used t-tests. Normality was tested using a Shapiro-Wilk's test (SAS 1991) and homogeneity of variances using a Levene test (Snedecor & Cochran 1989). LS means multiple pairwise comparisons were used to test a posteriori for specific differences when the ANOVAs indicated significant (P [less than or equal to] 0.05) differences (SAS 1991).

RESULTS

Masses of Bad), Components

During the period from May 30 to August 14, 2000, marked changes in the wet and dry mass of gonad and somatic components were apparent, particularly in male scallops (Fig. 1). These changes occurred despite a lack of difference in shell height of the males sampled on these dates (P = 0.68). The wet and dry mass of the testes and ovary increased markedly between May 30 and July 20 and decreased precipitously by August 14, indicating gonad maturation and spawning, respectively. Testis dry mass was significantly (P = 0.018) larger than ovarian dry mass on May 30. This suggests that gonad maturation was advanced in males relative to females. Such a pattern was observed for this population of C. islandica during the reproductive seasons of 1990 and 1991 (D. Arsenault, personal communication). At maturity, the wet mass of the ovaries was greater than that of the testes (P = 0.0005), although dry masses were similar (P = 0.53), suggesting that ovaries are more hydrated when fully mature. In females, during maturation and spawning most body components (wet and dry masses) remained stable (P > 0.05), with the exception that the dry mass of the remaining tissues (mainly mantle and gills) was lowest after maturation and increased after spawning (P < 0.05) (see Fig. 1). In males, during gonad maturation and spawning, the digestive gland mass decreased steadily, attaining its lowest value after spawning (P < 0.05). Adductor muscle dry mass dropped (P < 0.05) during testis maturation and recovered slightly after spawning, whereas the mass of the remaining tissues stayed constant (see Fig. 1).

[FIGURE 1 OMITTED]

No sex differences in the mass of the adductor muscle, digestive gland, and remaining tissues were observed (P > 0.05) before and after gonad maturation. However, after spawning, the wet and dry masses of the adductor muscle, digestive gland, and remaining tissues were lower (P < 0.05) in males than in females. This difference was not significant for the digestive gland when measured as dry mass (P = 0.059).

Biochemical Components

During gonad maturation, the absolute contents of carbohydrate and protein in ovary and testis increased markedly. Lipid levels only increased in the ovary (Fig. 2). In parallel, glycogen in the adductor muscle decreased by 160 and 185 mg in females and males, respectively, carbohydrates in the remaining tissues dropped by 70 and 66 mg in females and males respectively, and male scallops showed a 15 mg decrease of digestive gland carbohydrates. In contrast, the carbohydrate content of the female digestive gland increased by 19 mg during maturation (see Fig. 2). During gonad maturation, protein contents remained constant in all somatic tissues, and somatic lipids only decreased in the male digestive gland (467 nag) (see Fig. 2).

[FIGURE 2 OMITTED]

After spawning, all biochemical components of the ovary and testis dropped to their lowest levels (see Fig. 2). In female and male scallops, muscle carbohydrate remained low, however carbohydrate in the remaining tissues returned to pre-maturation levels. Protein levels in the digestive gland decreased by 80 mg with spawning of male scallops, whereas lipid levels decreased by 288 and 400 mg in females and males, respectively (see Fig. 2).

Energetic Changes During Maturation

During the period of ovary maturation we studied, female somatic components lost a total of 4 kJ (taking only statistically significant variations into account), while the ovary gained 41.5 kJ (Table 1). Thus, somatic tissues contributed only I0% of the energetic gain of ovaries. Adductor muscle provided 70% and the remaining tissues 30% of this energy. Only carbohydrate was responsible for the energetic loss of somatic tissues in females. If the decrease in lipids in the digestive gland, even though it was not significant, is included in this calculation, 25% of the ovarian energy gain was explained.

During the period of testis maturation we studied, somatic tissues lost a total of 21 kJ, while testis gained 17 kJ (Table 2). Therefore, the energetic gain of the testis was completely supported by somatic tissues. Digestive gland accounted for 80%, adductor muscle 15%, and the remaining tissues 5% of the total caloric loss in the somatic tissues during testes maturation. In the digestive gland 99% of the energetic reduction was caused by lipid loss and 1% to carbohydrate loss. The total caloric loss in the adductor muscle and remaining tissues was caused by carbohydrate. The remaining tissues also showed a marked reduction of lipid but, as in the digestive gland, this was not statistically significant.

During the period of gonad maturation we studied, somatic proteins made no energetic contribution in males or females. In males, lipids represented 78% and carbohydrates 22% of somatic energy loss. In females, only carbohydrate reserves showed statistically significant changes. Although the energetic gain in the ovary was more than 2-fold that of the testis, the increments in protein and carbohydrate were similar in both gonads (see Tables 1 and 2). The difference in energy gain reflected the marked increase in ovarian lipids, whereas the change in testicular lipids was not significant.

Energetic Changes With Spawning

During spawning, the ovary lost 73 kJ and testis 49 kJ, confirming the greater energetic investment in egg production. The remaining tissues in females and males increased their caloric content, mainly because of the recovery of initial carbohydrate levels (see Tables 1 and 2). Adductor muscle energy contents did not change. On the other hand, the energy content of the digestive gland dropped to its lowest level in females and males, mainly caused by lipid loss. Thus, the somatic contribution to energy requirements during spawning came from digestive gland lipids in female and male C. islandica. The total energetic decrease during spawning was 83.5 kJ in females and 65.2 kJ in males.

DISCUSSION

In the Mingan Islands, gonad maturation and spawning of C. islandica was accompanied by changes in body mass and biochemical components that differed markedly between males and females. Although spawning led to a considerably greater energy loss in female than in male gonads (73 vs. 49 kJ in gonad energy content), less mobilization of somatic energy was observed during gonad maturation and spawning in females than males (4 vs. 21 kJ during maturation and 10.5 vs. 15.7 kJ with spawning). The sex difference in investment during maturation (41.5 10 vs. 17 kJ) was accentuated by the fact that the testes were larger than the ovaries at the start of our study, due to an advanced gametogenesis in males (Arsenault & Himmelman 1998). However, despite their greater reproductive investment, female scallops showed less somatic energy mobilization. Most of" the energy requirements for ovarian maturation must have been covered by feeding, whereas somatic reserve mobilization could have covered the costs of maturation in males.

The sex differences in the changes of somatic reserves during gonad production and spawning were opposite those we predicted. What factors could explain the observation that female scallops can support the production of energetically expensive ovarian tissue by feeding, whereas males break down somatic tissues? Because the male and female scallops were sampled in the same habitat, food availability did not differ. If sperm production increases metabolic rate more than egg production, then the availability of aerobic power for food assimilation could be reduced thereby limiting feeding. Because the metabolic rate of mature male C. islandica is higher than that of mature females (Vahl & Sundet 1985), the aerobic scope available for feeding and assimilation could be lower in males than females. Protein levels increased more in the testes than in the ovaries during maturation, whereas lipids increased only in ovaries (see Fig. 2). De novo protein synthesis for sperm production is likely to be more costly than lipid deposition in the yolk. Protein synthesis requires activation of amino acids during their incorporation into nascent polypeptides and may require production of the appropriate amino acids. Because dietary fatty acids can be directly esterified into triglycerides and phospholipids, the energetic cost of lipid absorption and deposition is lower than the calorific value of the lipids. The close morphologic association between the digestive gland and the gonad could facilitate the direct transfer of lipids from food to gametes. Whereas these mechanistic explanations for the sex difference in breakdown of somatic reserves are speculative, our results suggest that male survival may be decreased by their reproductive investment whereas female scallops maintain greater survival and hence future reproduction.

In female C. islandica, the energetic gain by the ovary (41.5 kJ) during its growth was ~10 fold greater than the energetic loss in somatic tissues (muscle + digestive gland + "remaining tissues" = 4.0 kJ) (see Table 1). Even if the lipid change in the digestive gland (not significant) is taken into account, energy gain by the gonad was 4-fold the loss of somatic tissues. Therefore, because energy loss by somatic tissues must have accounted for only a small fraction of ovarian growth, external food supplies covered the remainder of this growth. The fact that, in C. islandica from the Mingan Islands, most ovarian maturation occurs during the spring-summer peaks of food concentration (Spence & Steven 1974, Arsenault & Himmelman 1998, and Brokordt et al. 2000a) suggests this is feasible. This is not what occurs in Pecten maximus, in which gonad growth takes place during the winter, and in which the energy loss by the adductor muscle was 23% larger than energy gain by the gonad (no differences were made between sexes because P. maximus is a hermaphrodite) (Faveris & Lubet 1991). Thus adductor muscle reserves in P. maximus support not only gonad growth but also maintenance requirements, maybe because of low food availability during winter. These observations in P. maximus are similar to our results for male C. islandica. In summary, during gonad maturation, female C. islandica only mobilized carbohydrate reserves, mainly from muscle but also from the remaining tissues. Males mobilized both lipids (from the digestive gland) and carbohydrates (from all somatic tissues, but mainly from muscle), but lipid mobilization was more important in terms of amount (rag) and energy content (kJ). Therefore, the energetic support of ovarian maturation was carbohydrate based whereas testis maturation was primarily lipid based. During spawning, energetic demands in females and males are mainly supported by lipids from the digestive gland, but again males made a bigger somatic effort, losing 15.7 kJ versus a loss of 10.5 kJ in females (see Tables 1 and 2). Therefore, somatic energy loss during gonad growth and spawning was 2.5-fold greater in male than in female C. islandica (36.7 kJ and 14.5 kJ, respectively). Again this suggests that reproduction would reduce survival more in male than female scallops.

We analyzed the changes of biochemical components in the body tissues during gonad maturation and spawning in 13 species of scallops (Table 3) to compare with our results for C. islandica and to seek a common pattern for scallops. This compilation included species from different geographic zones and different degrees of biochemical analysis (not all of them included all somatic tissues or biochemical substrates). Most of the scallop species studied (11 of 13), used one or more energy reserves during gonad maturation. The two exceptions were Chlamys septemradiata from the Clyde Sea, England (Ansen 1974), and Nodi Pecten subnodosus from Bahia Magdalena, Mexico (Racotta et al. 2001), species that increased biochemical components in all somatic tissues during gonad maturation. In these species, gonadal growth was supported directly and only by feeding. Other partial exceptions are some species or populations that have more than one reproduction or partial spawning per year, like P. maximus and Aequi Pecten opercularis from Ria de Arousa (Galicia, Spain) (Pazos et al. 1997 and Roman et al. 2003) and Chlamys varia (Shafee 1981), in which spring gametogenesis and spawning are usually supported by external food supplies, which are abundant during this season. In contrast, autumn or winter reproduction in all the three species is supported by somatic tissue reserves. As a general pattern, and as found in female C. islandica, most species use carbohydrates (9 of II), mainly from muscle and (8 of 9) as an energy substrate for supporting gonad maturation. Lipid and protein reserves were equally used during gonad growth (6 of 11) lipids coming mainly from the digestive gland (4), and proteins from adductor muscle (4). Reliance on muscle and mantle proteins is particularly pronounced in the semelparous A. irradians concentricus (Barber & Blake 1981) and A. irradians irradians (Epp et al. 1988). Thus, the literature shows that adductor muscle is the most important storage tissue providing energy substrates for gonad maturation in scallops, but that the extent of mobilization and the reserve used depends on food availability during maturation and the reproductive strategy (single vs. multiple spawners).

Of the 13 studies we analyzed, 10 evaluated the changes of biochemical components in body tissues during spawning (see Table 3). In stone species, spawning is accompanied by recuperation of energy substrates depleted during gonad growth. This occurred in Pecten maximus from the Bale de Seine, Erauce (Faveris & Lubet 1991), in C. varia from Bretagne, France (Shafee 1981), Argopecten irradians irradians from New York, United States (Epp et al. 1988), and for mantle carbohydrates in male and female C. islandica (present study). However, most scallop species continue depleting the same biochemical reserves that were used during gonad maturation, or used reserves that were not used during gonad growth, to support energy demands during spawning. This was seen in C. islandica, C. septemradiata, Placopecten magellanicus from Nova Scotia, Canada (Couturier & Newkirk 1991), A. irradians concentricus from the Gulf of Mexico, United States (Barber & Blake 1981), E. ziczac from the Golfo de Cariaco, Venezuela (Brokordt et al. 2000b), A. purpuratus from Coquimbo, Chile (Martinez 1991 and Martinez el al. 2000) and Lyropecten (Nodipecten) nodosus from the Golfo de Cariaco, Venezuela (Lodeiros et al. 2001). As during gonad maturation, adductor muscle reserves were most frequently used during spawning (5 of 10 species, Table 4). However, here muscle carbohydrates and proteins were of similar importance (4 and 3 species, respectively), followed by lipid reserves (4 of 10 species) from all three somatic tissues.

The reliance of scallops on the adductor muscle as an energy storage site has been suggested to reflect the monomyarian condition, which requires a readily available source of energy to support muscle contraction during swimming and escape responses (Ansell 1974). Muscle contraction is initially supported by ATP production from arginine phosphate, with octopine production from glycogen occurring in the final stages of exhaustive escape responses (Thompson el al. 1980, Livingstone et al, 1981, Chih & Ellington 1983, and Chih & Ellington 1986). The escape response and swimming performance would thus be largely maintained even after reduction of muscle glycogen levels. Recuperation from exhaustion relies on glycolytic breakdown of glycogen with ensuing octopine production (Thompson et al. 1980, Livingstone et al. 1981, Chih & Ellington 1983, and Chih & Ellington 1986). The preferential mobilization of carbohydrates for gonadal growth should primarily slow the capacity to renew escape responses. Effectively, the marked reduction of muscle glycogen during gonad maturation in C. islandica and E. ziczac is paralleled by decreases in muscle metabolic capacities anti in recuperation from exhaustive exercise (Brokordt et al. 2000a and Brokordt et al. 2000b). On the other hand, in most scallops the adductor muscle contains 2-10-fold more protein than carbohydrate, suggesting that the mobilization of an energetically equivalent quantity of protein would cause a proportionally smaller impact on adductor muscle performance. However, several factors argue against the use of protein. Muscle proteins have functional roles that make them art energetic reserve of last resort. Thus, mobilization of structural proteins (50%-60% of muscle proteins in C. islandica and E. ziczac (Brokordt et al. 2000a and Brokordt et al. 2000b) would reduce muscle integrity. Even though soluble proteins are twice as abundant as muscle glycogen in C. islandica (Borkordt et al. 2000a), glycogen is used first, likely a reflection of the functional importance of these soluble proteins. Furthermore, the degradation of glycogen into sugar units and their use for the production of gonad carbohydrates or triglycerides would be metabolically simpler and energetically cheaper than the breakdown and resynthesis of proteins. Similar arguments underlie the use of lipids during ovocyte production. Explanations of the metabolic strategies underlying inter-tissue transfers of material and energy and reliance on dietary sources must integrate not only the energetic value of the components and the functional consequences of their use (ie, decreased behavioral responses) but also the energetic cost of their production.

TABLE 1.
Caloric (kJ) content in the biochemical components of tissues of
female Chlamys islandica, in different reproductive stages, and
significant (P < 0.05) caloric losses and gains ([DELTA]E) after
gonad maturation and spawning.

Reproductive                              Carbohydrate
   Stage       Protein     [DELTA]E          Muscle

Immature        44.6                           5.3
Mature          45.7       1.2 (n.s.)          2.6
Spawned         43.6      -2.1 (n.s.)          2.7
                                         Digestive Gland
Immature         4.3                           0.5
Mature           4.5       0.2 (n.s.)          0.8
Spawned          3.7      -0.8 (n.s.)          0.5
                                        Remaining Tissues
Immature        10.6                           1.5
Mature          11.6       1.0 (n.s.)          3.0
Spawned         10.9      -0.8 (n.s.)          1.3
                                              Gonad
Immature        20.1                           3.4
Mature          31.3      11.2                 5.8
Spawned          6.3     -25.0                 1.8

Reproductive
   Stage        [DELTA]E     Lipid     [DELTA]E

Immature                     n.e.
Mature         -2.8          n.e.
Spawned         0.1 (n.s.)   n.c.

Immature                     20.7
Mature          0.3          15.3     -5.4 (n.s.)
Spawned        -0.3           5.1    -10.2

Immature                     26.2
Mature         -1.2          26.7      0.5 (n.s.)
Spawned         1.0          30.2      3.5 (n.s.)

Immature                     35.3
Mature          2.4          63.2     27.9
Spawned        -4.0          19.2    -44.0

Reproductive   [summation of]   [summation of]   [summation of]
   Stage         Substrate         [DELTA]E         E Losses

Immature            49.9
Mature              48.3             -2.8             -2.8
Spawned             46.3              0                0

Immature            25.5
Mature              20.6              0.3              0
Spawned              9.3            -10.5            -10.5

Immature            38.3
Mature              38.6              0.3             -1.2
Spawned             42.3              1.0              0

Immature            58.7
Mature             100.3             41.5              0
Spawned             27.3            -73.0            -73.0

(n.s. = not significantly different. P < 0.05, n.e. = not evaluated)

TABLE 2.
Caloric (kJ) content in the biochemical components of tissues of male
Chlamys islandica, in different reproductive stages, and significant
(P < 0.05) caloric losses and gains ([DELTA]E) after gonad maturation
and spawning.

Reproductive                              Carbohydrate
   Stage       Protein     [DELTA]E          Muscle

Immature        39.2                           5.1
Mature          37.8      -1.4 (n.s.)          2.0
Spawned         42.0       4.2 (n.s.)          1.8
                                         Digestive Gland
Immature         4.7                           0.7
Mature           4.7       0.0                 0.5
Spawned          3.1       1.6                 0.4
                                        Remaining Tissues
Immature        11.8                           1.3
Mature          12.0       0.1 (n.s.)          0.2
Spawned         10.1      -1.8 (n.s.)          1.1
                                              Gonad
Immature        17.1                           3.1
Mature          11.9      14.8                 5.3
Spawned          7.6     -24.3                 1.9

Reproductive
   Stage         [DELTA]E     Lipid     [DELTA]E

Immature                      n.e.
Mature          -3.2          n.e.
Spawned         -0.2 (n.s.)   n.e.

Immature                      35.3
Mature          -0.3          18.8    -16.5
Spawned         -0.1 (n.s.)    4.7    -14.2

Immature                      30.3
Mature          -1.1          23.8     -6.0 (n.s.)
Spawned          0.9          29.3      5.6 (n.s.)

Immature                      34.2
Mature           2.2          35.8      1.6 (n.s.)
Spawned        -33.0          14.2    -21.6

Reproductive   [summation of]   [summation of]   [summation of]
   Stage         Substrate         [DELTA]E         E Losses

Immature            44.4
Mature              39.7             -4.6             -4.6
Spawned             43.7              4.0             -0.2

Immature            40.8
Mature              24.1            -16.7            -16.7
Spawned             8.2             -15.8            -15.8

Immature            43.5
Mature              35.9             -7.6             -7.7
Spawned             40.6              4.6             -1.8

Immature            54.4
Mature              73.0             18.7              0
Spawned             23.7            -49.3            -49.3

(n.s. = not significant different. P < 0.05, n.e. = not evaluated)

TABLE 3.
Changes of biochemical components in the body tissues during gonad
maturation and spawning in thirteen species of scallops.

         Species                     Gonad Maturation

Chlamys septemradiata         [up arrow] Muscle carbohydrate
                              [up arrow] Mantle carbohydrate
                              [up arrow] Muscle lipid
                              [up arrow] Mantle lipid
                              [up arrow] Muscle protein
                              [up arrow] Mantle protein
Chlamys islandica
  Female                    [down arrow] Muscle carbohydrate
                            [down arrow] Remaining tissues carbohydrate
                              [up arrow] Digestive gland carbohydrate
  Male                      [down arrow] Muscle carbohydrate
                            [down arrow] Remaining tissues carbohydrate
                            [down arrow] Digestive gland carbohydrate
                            [down arrow] Digestive gland lipid
Pecten maximus              [down arrow] Muscle carbohydrates
                            [down arrow] Muscle lipid
                            [down arrow] Muscle protein
C. varia                    [down arrow] Somatic carbohydrate
                            [down arrow] Somatic lipid
Placopecten magellanicus      [up arrow] Muscle carbohydrate
                            [down arrow] Muscle protein
Aequipecten opercularis     [down arrow] Muscle carbohydrate
                            [down arrow] Muscle protein
                            [down arrow] Digestive gland lipid
A. irradians irradians      [down arrow] Muscle lipid
                            [down arrow] Muscle protein
                            [down arrow] Mantle protein
A. irradians concentricus   [down arrow] Muscle carbohydrate
                            [down arrow] Muscle protein
                            [down arrow] Mantle protein
                            [down arrow] Digestive gland lipid
A. ventricosus              [down arrow] Muscle carbohydrate
                              [up arrow] Muscle protein
                              [up arrow] Digestive gland protein
Nodipecten subnodosus         [up arrow] Muscle carbohydrate
                              [up arrow] Muscle protein
                              [up arrow] Mantle carbohydrate
                              [up arrow] Digestive gland carbohydrate
                              [up arrow] Digestive gland lipid
                              [up arrow] Digestive gland protein
Euvola ziczac               [down arrow] Muscle carbohydrate
Liropecten nodosus          [down arrow] Muscle carbohydrate
                              [up arrow] Muscle lipid
                            [down arrow] Remainder tissues carbohydrate
                              [up arrow] Digestive gland lipid
Argopecten purpuratus       [down arrow] Muscle carbohydrate
                              [up arrow] Muscle protein
                              [up arrow] Muscle protein

         Species                         Spawning

Chlamys septemradiata       [down arrow] Muscle carbohydrate
                            [down arrow] Mantle carbohydrate
                            [down arrow] Muscle lipid
                            [down arrow] Mantle lipid
                            [down arrow] Muscle protein
                            [down arrow] Mantle protein
Chlamys islandica
  Female                      [up arrow] Remaining tissues carbohydrate
                            [down arrow] Digestive gland carbohydrate
                            [down arrow] Digestive gland lipid
  Male                        [up arrow] Remaining tissues carbohydrate
                            [down arrow] Digestive gland carbohydrate
                            [down arrow] Digestive gland lipid
Pecten maximus                [up arrow] Muscle carbohydrate
                              [up arrow] Muscle lipid
                              [up arrow] Muscle protein
C. varia                      [up arrow] Somatic carbohydrate
                              [up arrow] Somatic lipid
Placopecten magellanicus    [down arrow] "Other tissues" protein
Aequipecten opercularis
A. irradians irradians        [up arrow] Muscle lipid
                              [up arrow] Muscle protein
A. irradians concentricus   [down arrow] Muscle protein
A. ventricosus
Nodipecten subnodosus
Euvola ziczac               [down arrow] Muscle carbohydrate
                            [down arrow] Muscle protein
Liropecten nodosus          [down arrow] Muscle carbohydrate
                            [down arrow] Remainder tissues protein
                            [down arrow] Digestive gland lipid
Argopecten purpuratus       [down arrow] Muscle carbohydrate
                            [down arrow] Muscle lipid
                            [down arrow] Mantle carbohydrate
                            [down arrow] Mantle lipid

         Species                    Source

Chlamys septemradiata       Ansell 1974
Chlamys islandica           Brokordt et al 2000
  Female                      (present study)
  Male
Pecten maximus              Faveris & Lubet 1991
C. varia                    Shafee 1981
Placopecten magellanicus    Couturier & Newkrk 1991
Aequipecten opercularis     Taylor & Venn 1979,
                            Roman et al. 2001
A. irradians irradians      Epp et al. 1998
A. irradians concentricus   Barber & Blake 1981
A. ventricosus              Chavez, unpubl. data
Nodipecten subnodosus       Racotta et al. 2001
Euvola ziczac               Brokordt et al. 2000
Liropecten nodosus          Lodeiros et al. 2001
Argopecten purpuratus       Martinez 1991,
                            Martinez et al. 2001

Table 4.
Proportion of scallop species (n = 13) using different biochemical
components (and the primary source tissue) to support gonad
maturation and spawning.

Reproductive
  Process       Carbohydrates         Proteins            Lipids

Gonad          82% (88% muscle)   55% (66% muscle)   55% (70% muscle)
maturation

Spawning       50% (80% muscle)   50% (60% muscle)   40% (from all
                                                     three tissues)

ACKNOWLEDGMENTS

This study was supported by a grant from NSERC to HG. The authors thank Dominique Lapointe and Marie-Eve Fortin for careful technical assistance and to Martin Guay for the sampling of the scallops.

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KATHERINA B. BROKORDT (1,2) AND HELGA E. GUDERLEY (1), *

(1) Departement de Biologic and Quebec- Ocean, Universite Laval, Quebec City, Quebec G1K 7P4, Canada; (2) CEAZA (Centro de Estudios Avanzados en Zonas Aridas), Casilla 599, Let Serena, Chile, and Departamento de Ecologia, Pontificia Universidad Catolica de Chile, Alameda 340, Santiago, Chile 

* Corresponding author. E-mail address: [e-mail].