The effect of depth on the reproductive and reserve storage cycles of the pectinids Aequipecten opercularis (L., 1758) and Chlamys varia (L., 1758) in Galicia, Northwest Spain.
Article Type: Report
Subject: Scallops (Physiological aspects)
Growth (Research)
Authors: Iglesias, Paula
Louro, Angeles
Roman, Guillermo
Pub Date: 08/01/2012
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2012 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: August, 2012 Source Volume: 31 Source Issue: 3
Topic: Event Code: 310 Science & research
Product: Product Code: 0913070 Scallops NAICS Code: 114112 Shellfish Fishing SIC Code: 0913 Shellfish
Geographic: Geographic Scope: Spain Geographic Code: 4EUSP Spain
Accession Number: 303011390
Full Text: ABSTRACT Spat of 2 pectinid species of commercial interest were grown in suspension to study the growth of the gonad, digestive gland, and adductor muscle at 3 different depths (2.5 m, 7.5 m, and 12.5 m). For the experiments, we used spat immediately after they were detached from the collectors (Aequipecten opercularis) or 3-4 mo later (Chlamys varia). The first sexual maturation of each species was recorded. The variations observed in the gonad development pattern were clearly a result of the effect of depth on the gonad growth of the 2 species. Both species showed faster gonad development at 2.5 m. Reproduction of C. varia was more intense in deeper water. This was also the case for A. opercularis in the first reproduction period, from the end of winter to early summer. After a resting period in summer, there was a first peak of gonad growth at 2.5 m in October that did not occur at 7.5 m and 12.5 m. There was a peak in January at all depths. The reserve storage organs of both A. opercularis and C. varia showed a regular pattern of evolution. In general, the variations in the reserve organs followed the same pattern at all depths with 2 exceptions: the digestive gland in C. varia in spring at 2.5 m, which showed a faster growth rate related to higher temperatures; and the digestive gland and muscle in A. opercularis, which showed a large growth peak in late spring and early summer at 12.5 m that did not occur at other depths and that was related to lower temperatures and greater food availability. The growth of the reserve organs was more conservative despite the variations in the environmental conditions that occurred during the experimental period. Gonad growth was affected more by environmental changes, and was more versatile.

KEY WORDS: scallop, Aequipecten opercularis, Chlamys varia, depth, temperature, food availability, reserve storage organs, gonad, spawning

INTRODUCTION

Scallops grown in suspension are subjected to different environmental conditions in relation to the distinct temperatures, salinities, and food availability that occur at different depths in the water column. The depth at which the scallops are cultured can therefore affect growth of both the shell and the soft parts.

Environmental conditions can influence the reproductive and reserve storage cycles in different ways, as temperature and food availability are the main factors involved in regulating the gametogenic cycle in Pecten maximus (Roman & Acosta 1990), Euvola ziczac, (Brea 1986) Argopecten ventricosus (Luna-Gonzalez 1997) Argopecten irradians (Barber & Blake 1981), and Placopecten magellanicus (MacDonald & Thompson 1985).

The effect of depth on growth and reproduction has been reported for several pectinid species. Both shell (Mason 1957, Broom & Mason 1978, Posgay 1979, MacDonald & Thompson 1985, MacDonald & Thompson 1988, Schick et al. 1988, Smith et al. 2001, Hart & Chute 2004, Hart & Chute 2009) and soft tissue growth (Smith et al. 2001, Lai & Helser 2004, Hart & Rago 2006) decrease with depth, probably as a result of the lower levels of phytoplankton in deeper water. Depth affects the reproduction of different species differently. Barber et al. (1988), Schmitzer et al. (1991), and MacDonald & Thompson (1986), who studied P. magellanicus, and Skreslet Brun (1969), who studied Chlamys islandica, found that gonad indexes decreased as depth increased, whereas Roman et al. (1999) and Campos et al. (2001) found that gonad growth decreased in Aequipecten opercularis grown in shallower water. However, Parada et al. (1993) did not find any significant differences in the gonad indexes in Chlamys varia grown between 1 m and 7 m.

The objectives of this experiment were to study the response of 2 pectinids cultured in suspension at 3 different depths and subjected to variable conditions. The results of the study were used to gain a better understanding of the requirements of A. opercularis and C. varia to optimize the meat yield, determine better breeding stock handling practices and, as a future objective, manage the participation of the cultured stock in the annual recruitment.

MATERIALS AND METHODS

Two commercially valuable species present in Galician waters, northwest Spain, were used in the experiment: the black scallop, C. varia, and the queen scallop, A. opercularis. All the animals used were obtained from spat that settled on collectors. The scallop A. opercularis settled on collectors placed in May and June 2007 in Ria de Aldfin, Pontevedra. Spat were detached in September and kept in hanging cages before the experiments started. Experiments started on October 16, 2007 (initial height, 29.2 [+ or -] 1.9 mm). The spat of C. varia settled on collectors placed during spring and summer 2007 in Ria de Ares-Betanzos, A Coruna. They were detached in autumn and winter and were kept in hanging cages. Experiments started on April 17, 2007, when the spat had a mean size of 26.4 [+ or -] 6.7 mm in height. Both species were cultured in the rias where they settled (Fig. 1).

In all cases, the spat were grown in trays with a diameter of 40 cm that were hung from a raft, placed at depths of 2.5 m, 7.5 m, and 12.5 m. Greater depths were not tested because, as depth increases, the ropes become entangled and make culture operations difficult. For each depth, 3 groups of 6 trays with 60 scallops per tray were used. For sampling, roughly every 2 wk, 8-9 scallops of 1 tray from each group of trays were picked up randomly until a total of 25 scallops had been acquired. Every other month in spring and summer, and every 3 mo in autumn and winter the fouled trays were removed and the scallops were placed on clean ones, adjusting scallop density to 60 per tray. After collecting, the scallops were transported to the laboratory and the shell height was then measured. The gonad, adductor muscle, and digestive gland were dissected, and the dry weight of organs was recorded after drying in an oven at 100[degrees]C until constant weight was achieved. Shell weight was recorded after 48 h at room temperature. Condition indexes (CIs), according to the equation Organ CI = 100 x [Organ dry weight/Shell dry weight] were used to monitor the variation in the gonad condition index (GCI) and the somatic tissues over time (muscle condition index (MCI), digestive gland condition index (DGCI)), because they describe the breeding cycle and the reserve storage and use cycles over time, respectively. Integrated (0-5 m, 5-10 m, and 10-15 m) temperature, salinity, and chlorophyll a values of the water column were recorded weekly with a CTD SEABIRD 25 immersed in a point close to the rafts.

[FIGURE 1 OMITTED]

RESULTS

Environmental Conditions in the Ria de Aldin

Temperatures were similar at all 3 depths from October 2007 to April 2008. From April to September, and especially from June to September, temperature can differ by 4[degrees]C between 2.5 m and 12.5 m. Differences were not as pronounced between 7.5 m and 12.5 m, with a maximum difference at 7.5 m of 1.3[degrees]C in May; most of the time there was a difference of roughly 0.4[degrees]C. In spring and summer, significantly higher temperatures were recorded at 2.5 m (means, 15.2[degrees]C in spring, 17.4[degrees]C in summer) than at 7.5 m and 12.5 m (means of 14.6[degrees]C and 14.3[degrees]C in spring, 15.9[degrees]C and 15.4[degrees]C in summer, respectively, at 7.5 m and 12.5 m; 1-way ANOVA, P < 0.005; Fig. 2A).

Throughout the year, salinity generally ranged between 35 psu and 35.8 psu. Although it decreased on April 28 at 2.5 m to a minimum value of 32.1 psu, no significant differences were recorded among the 3 depths.

[FIGURE 2 OMITTED]

Food availability was measured as a level of chlorophyll a. Similar values were recorded at all depths from the beginning of the experiment until spring. From spring to autumn, the highest values were recorded at 12.5 m (means, 7.6 [micro]g chlorophyll a/L and 8.4 [micro]g chlorophyll a/L in spring and summer, respectively), and the lowest values were recorded at 2.5 m (means, 2.4 [micro]g chlorophyll a/L and 3.3 [micro]g chlorophyll a/L in spring and summer, respectively). These differences were significant in spring at P < 0.005 (1-way ANOVA, 12.5 m > 7.5 m > 2.5 m), whereas in the summer only the values recorded at 2.5 m were significantly lower than those recorded at 7.5 m and 12.5 m (Fig. 3A).

Environmental Conditions in the Ria de Ares-Betanzos

The warmest temperatures were recorded at 2.5 m, and were as much as 3.2[degrees]C warmer than temperatures at 7.5 m and 12.5 m from June to September. Slightly warmer temperatures (roughly 0.5[degrees]C higher) were recorded at 7.5 m than at 12.5 m, except in August, when differences of more than 1[degrees]C were observed. In spring and summer, the water temperature was significantly warmer at 2.5 m (means, 15.6[degrees]C in spring, 18.1[degrees]C in summer) than at 7.5 m and 12.5 m (means, 15.0[degrees]C and 14.7[degrees]C in spring, 16.7[degrees]C and 16.3[degrees]C in summer at 7.5 m and 12.5 m, respectively; 1-way ANOVA, P < 0.005; Fig. 2B).

Most of the year, salinity ranged between 35 psu and 35.5 psu, although there were some decreases, especially at 2.5 m, and a minimum value of 32.4 psu was recorded on April 28 at that depth. In spring, the salinity was significantly lower at 2.5 m than at 12.5 m (means, 34.9 psu and 35.5 psu, respectively; 1-way ANOVA, P < 0.005).

Higher chlorophyll a values were generally recorded at 12.5 m. Significantly higher values were recorded in spring at 12.5 m (mean, 6.9 [micro]g chlorophyll a/L) than at shallower depths (means, 2.3 [micro]g chlorophyll a/L at 2.5 m and 3.7 [micro]g chlorophyll a/L at 7.5 m), whereas in summer the values were greater at 12.5 m (mean, 9.0 [micro]g chlorophyll a/L) than at 2.5 m (mean, 3.4 [micro]g chlorophyll a/L). Intermediate values were recorded at 7.5 m (1-way ANOVA, P < 0.005; Fig. 3B).

[FIGURE 3 OMITTED]

Shell Growth

Aequipecten opercularis

At the end of the experiment in January 2009, the scallops had reached a mean height of 51-53 mm. The highest growth rates were recorded in winter and spring, and decreased in summer and autumn. Although there was slightly less growth at 2.5 m, there were no significant differences in growth at the 3 tested depths (Fig. 4).

Chlamys varia

Growth was greater at 12.5 m and 7.5 m than at 2.5 m, and significant differences were recorded from the beginning of autumn. At the end of the experiment, December 2008, scallop height reached mean values of 41.6 [+ or -] 3.3 mm at 12.5 m, 42.2 [+ or -] 4.2 mm at 7.5 m, and more than 38.9 [+ or -] 3.1 mm at 2.5 m (1-way ANOVA, P < 0.005).

The scallop A. opercularis shows a greater growth rate than C. varia, reaching commercial size (from 50 mm upwards) after 1 y of suspension culture, whereas C. varia needed another year of culture to reach the commercial size (Iglesias, not publ.).

Gonad Growth

Aequipecten opercularis

In the study area, development of the first gonad began in autumn after the spring--summer settlement. Consequently, the gonad had already started to develop when the study began and the scallops were 5 mo old. The GCI showed an exponential growth rate in January, peaking at different dates according to the depth (Fig. 5A). Decreases in GCIs were considered as spawning if significant differences were recorded when values were compared with the previous value with 1-way ANOVA. Accordingly, the spawning period started on February 26 at 7.5 m, March 25 at 2.5 m, and April 15 at 12.5 m, and continued to the beginning of July, showing a different pattern at the 3 depths. At 2.5 m, there was a peak on March 25 (GCI, 2.40) and another on June 3 (GCI, 3.65). At 7.5 m, there were 3 peaks--February 26 (GCI, 2.14), April 15 (GCI, 2.72), and June 3 (GCI, 3.69), whereas at 12.5 m there were 2 peaks (GCI, 3.53 and 5.67), coinciding with the last 2 peaks at 7.5 m. At 7.5 In and 12.5 m, as the season proceeded, the peaks became larger and the values deceased more sharply, indicating that more gametes had been released. After June, the gonads had released all the gametes at all depths, and the minimum values of the year were reached on July 29 (GCI, 0.14-0.51), when a resting period began. At 2.5 m, new gonad growth was recorded, with a maximum value (GCI, 2.67) on September 25. Gonad development appeared to stop at 7.5 m and 12.5 m, and after an oscillating pattern, there was no full gonad development in the entire population until January 8, when values were very similar at all depths (GCI range, 2.08-2.54).

[FIGURE 4 OMITTED]

The maximum GCI, which was significantly greater than any other value, was recorded at 12.5 m on June 3, after a period when the seawater temperature was significantly colder and chlorophyll a values were significantly greater than at all the other depths.

Chlamys varia

When the experiment started in April, the gonad had already begun to develop. Gonad growth was slower at 7.5 m and 12.5 m, but on May 27, the GCI showed similar values at all depths (GCI, 2.00-2.17). Although at 2.5 m the gonad continued growing until it reached a maximum on June 10 (GCI, 2.78), at 12.5 m there was a small but significant decrease in value, probably associated with a first spawning. Spawning also started on this date at 7.5 m, whereas spawning started on June 10 at 2.5 m. The scallops kept at 2.5 m and 7.5 m spawned during June; the scallops at 7.5 m continued to spawn until August 4, whereas the scallops kept at 2.5 m continued to spawn intensely during the first half of September. Conversely, at 12.5 m, the gonad recovered after spawning in May until it reached a new maximum on July 9. After an increase in temperature between 10 June and 23 June (from 16.8 18.4[degrees]C), spawning was recorded at 12.5 m, which ended on 4 August. A significant minimum GCI value was recorded on this date in the scallops kept at 7.5 and 12.5 m depths, then the GCI increased significantly at these depths, at a faster but less intense rate at 7.5 m. After the gonad recovered during the first half of September, there was a complete release of gametes. The gonad then entered the resting phase until the next season (Fig. 5B).

[FIGURE 5 OMITTED]

At 2.5 m, a continuous breeding season was recorded that started in late spring and ended at the end of the summer. At 7.5 m and 12.5 m, a main spawning period took place between late spring and early summer. A second, shorter and faster, spawning started on September 1 (the deeper, the more intense), ending in the middle of September. At 7.5 m and 12.5 m, spawning started after the seawater temperature reached 16.0[degrees]C.

Somatic Tissue Growth

Aequipeeten opercularis

A decrease was recorded both in the DGCI and MCI at the beginning of the study, probably related to the winter conditions when there is little food in the water and the energy required for metabolic maintenance and gonad development must be supplied by the energy stored in the muscle and digestive gland. From the middle of January, there was rapid and simultaneous growth of both the gonad and digestive gland, mainly at 12.5 m, where the DGCI reached the highest values of the spring simultaneously with the GCI. At 7.5 m, the digestive gland stopped growing in March, coinciding with the second spawning, but began growing again at the same time as the gonad, before the third spawning. Less growth was recorded at 2.5 m, where 2 peaks were observed simultaneously with the gonad maximum values (Fig. 6A). In general, the DGCI increases before spawning and decreases after spawning. After minimum values at all depths, in July the DGCI and GCI of the scallops kept at 2.5 m increased simultaneously, until spawning took place on September 25. It then decreased continuously until January, when minimum values were recorded. At 7.5 m and 12.5 m, gonad growth apparently stopped, and maximum values were noted in the DGCI in association with small peaks in the GCI that did not result in complete gonad development, suggesting that the energy transfer from the digestive gland to the gonad was interrupted. The winter decrease in the DGCI began on November 19 at both 7.5 m and 12.5 m, and was related to the beginning of the new gonad maturation.

[FIGURE 6 OMITTED]

After a decrease in winter, like the DGCI, the MCI increased continuously from January until reaching maximum values at the end of summer. It showed significantly higher values at 12.5 m between May and June, like the DGCI (Fig. 7A). The increase in the MCI in spring and summer appeared to be independent of gonad development. At 2.5 m, the maximum MCI was reached on September 9, and then muscle growth decreased suddenly as in the digestive gland. At 7.5 m and 12.5 m, a plateau was recorded between September 9 and November 19, before a rapid decrease to the minimum values in January. Values recorded in autumn at 7.5 m were significantly greater than the ones at 12.5 m.

[FIGURE 7 OMITTED]

Chlamys varia

When the study started in spring, both the MCI and DGCI showed low, decreasing values, because energy was being used either for metabolic maintenance or for fueling the gonad energy requirements. In fact, only on May 27, when the GCIs had reached the maximum spring values, did both the MCI and DGCI begin to increase. Both indexes maintained high values throughout the summer, while the gonad was spawning, and then began to decrease in autumn, while the gonad was spawning, and reached minimum values in winter, when the gonad was in the resting phase. Both the DGCI and the MCI showed the same pattern independent of the depth at which the scallops were kept, although in spring at 2.5 m the DGCI increased faster, probably as a result of the warmer temperatures (Figs. 6B and 7B).

DISCUSSION

Environmental Conditions

Warmer temperatures and lower chlorophyll a levels in shallower water were recorded in both areas in spring and summer. Although low salinity can be a risk when scallops are grown in suspension at shallow depths, the fluctuation range observed during the experiments did not affect the growth or the

metabolism of the scallops. According to the results obtained by Paul (1980a), who worked with A. opercularis, mortality should not be expected at the combinations of low salinity (32.6 psu) and temperature (16.4[degrees]C) that occurred in the current study. Consequently, we consider that the differences observed in the CIs the different organs were generated by variations in temperature and food availability.

Reproductive and Reserve Storage Patterns: General Trends

It can be expected that there will be differences in reproductive behavior between wild and suspension-cultured animals, because the environmental conditions in suspension culture are considered more favorable for growth--basically, greater food availability. In this regard, the reproductive and reserve storage cycles of A. opercularis have been described in a wild population from the nearby Ria de Arousa (Roman et al. 2002). In that population, the GCI showed 4 peaks (GCI, 1.81-2.05) at the beginning of the breeding season (late February to early March), and values decreased progressively as the season proceeded, until the last spawning at the end of July (GCI, 0.64-0.86). In the current study, the breeding season started either on similar dates (7.5 m and 2.5 m) or slightly later (12.5 m), and ended on the same date; however, only 2 (2.5 m and 12.5 m) or 3 peaks (7.5 m) were recorded, although they reached considerably higher values (3.53-3.65 at 2.5 m; 2.15, 2.72, and 3.67 at 7.5 m; and 3.57-5.68 at 12.5 m). During the winter, the CIs of the reserve organs of the wild population decreased for a longer period, and consequently the recovery took place later, in April. The peaks had lower values than those recorded in animals kept in suspension culture (compare DGCI, 1.4-1.7 vs. 2.5; and MCI, 7.0-8.5 vs. 9.0-11.0, in wild populations and suspension cultures, respectively).

There is no information about the reproductive cycle of wild populations of C. varia in Galicia. Two main spawning periods are usually reported in France and Ireland (Lubet 1959, Lucas 1965, Burnell 1983), with the first one generally occurring in May to June and the other occurring at the end of summer, which is comparable to the cycle we found at 7.5 m and 12.5 m, but not at 2.5 m, where a single, prolonged spawning cycle was recorded. The general behavior trends recorded in the wild scallops remained constant at the various experimental depths, although some differences were observed in relation to changes in environmental conditions.

Reproductive Patterns

Gametogenic processes require energy, which can be supplied directly by the ingested food or by the reserves stored previously in the digestive gland and muscle (Ansell 1974, Gabbot 1975, Barber & Blake 1983, Pazos et al. 1997). According to Bayne (1976), energy storage and gonad development cycles may occur simultaneously or they may be clearly separate. When gametogenesis takes place using energy stored in body tissues, a conservative pattern occurs, but when gametogenesis takes place when there is enough food in the water to provide the energy required by the process, an opportunistic pattern occurs. According to the pattern, energy can be allocated either to gonadic or somatic growth, which involves reserves being stored. Therefore, the different patterns can mask the immediate effect of food availability in the reproductive cycles of the different species.

We observed in the current study that A. opercularis uses the stored reserves in winter while the gonad is developing, but from January onward, the external energy provided by food is used for gonad and somatic tissue growth, even though gonad recovery takes place from July to September. Growth of the somatic tissues started to decrease in autumn. It began earlier at 2.5 m and occurred at the same time as the beginning of the next gonad growth period. At 7.5 m and 12.5 m, the decrease took place simultaneously with the gonad growth period that occurred in January of the second year. Metabolic maintenance can also be involved in the decrease in growth of somatic tissues from the end of autumn to winter, as the chlorophyll a values are at their lowest at this time of year.

In C. varia, in winter the stored energy is devoted only to metabolic maintenance, but by spring the gonad starts to develop at the expense of the somatic tissues. In April, when the study of C. varia began, gametogenic processes had already started at the expense of the muscle and digestive gland. The somatic tissues do not start growing until the gonad is fully developed by the end of spring, reaching maximum values in August and September, before they are used as substrate for metabolic maintenance in the following months because there is no gonadic development from September until the next spring.

According to our results, A. opercularis behaves conservatively in autumn and winter, and opportunistically in spring and summer. However, C. varia is opportunistic except for a short period at the beginning of spring, when the gonad starts to develop, when it is conservative. The use of intermediate strategies has been described previously for some species, such as Mytilus edulis (Bayne 1976) and C. varia (Shafee 1981).

Effect of Environmental Conditions on the General Trends

Deviations from the general trends related to environmental conditions were observed. In A. opercularis, the DGCI decreased from September 9 at 2.5 m, probably in relation to the low chlorophyll a values and to the increase in the GCI that only occurred at this depth. At 7.5 m and 12.5 m, the DGCI oscillated, although there was an increasing trend until November 19. The DGCI then decreased as a result of low chlorophyll a values and the GCI increase. It is interesting to observe the behavior of the gonad from the middle of August to the middle of October at the different depths. At 7.5 m and 12.5 m, gonad development stopped. At these depths there were sudden changes in temperature, which oscillated between 14.6[degrees]C and 17.8[degrees]C, whereas at 2.5 m there was a slow decrease from 18.1[degrees]C to 15.8[degrees]C. Although studies on the upper lethal temperature for A. opercularis have shown that mortality occurs between 19[degrees]C and 24[degrees]C (Paul 1980b), and McLusky (1973) suggested that 20[degrees]C was near the lethal temperature, the scallops were able to start gonad development at the warmer temperatures observed at 2.5 m, whereas at 7.5 m and 12.5 m gonad development stopped. Perhaps scallops at 2.5 m were acclimated to high temperatures whereas the scallops kept in deeper water were stressed by the sudden changes in temperature.

The GCI increased rapidly during winter, and spawning started shortly after peaks in chlorophyll a values were noted. The colder temperatures recorded in winter in this area do not seem to have affected the growth of the queen scallop negatively, as the fastest gonadic and somatic growth were recorded between February and April, when temperatures ranged from 13.5 14.5[degrees]C. In fact, the scallops started to spawn at 14.0-14.5[degrees]C, and spawning occurred at all depths while the seawater temperature oscillated between 14.0[degrees]C and 15.5[degrees]C. However, the warmer temperatures in summer and early autumn did have a negative effect, except at 2.5 m, where the scallops were acclimated to them. The resting period took place when the seawater temperature was warmest.

In spring at 12.5 m, when food availability is significantly greater and the temperature colder, the gonad, muscle, and digestive gland of A. opercularis grew simultaneously during the period of highest gametogenic activity. At shallower depths, where there is less food and the temperature is warmer, there was either a transfer of energy from the digestive gland to the gonad, or the environmental conditions were not sufficient for digestive gland growth. Consequently, the gonad, muscle, and digestive gland displayed significantly greater values at 12.5 m. Conversely, significantly lower DGCIs and MCIs were recorded at 2.5 m in July, when the temperature reached higher values than at the other depths (16.7-17.2[degrees]C vs. 13.8 16.1[degrees]C).

In Chlamys varia, the date of first spawning could be correlated with seawater temperature. Lucas (1965) proposed that 15[degrees]C is the minimum spawning temperature of C. varia, whereas Burnell (1983) found that the decrease in the summer GCI usually coincided with a small temperature increase of 1-2[degrees]C up to 15.5[degrees]C or 16.0[degrees]C. Our results agree with theirs, as the gonads in the scallops kept at 7.5 m and 12.5 m started to release their gametes in May, immediately after the seawater temperature reached 16.0[degrees]C. This was not the case with scallops kept at 2.5 m, which started spawning later, in June at 16.5[degrees]C. It is possible that not only a minimum temperature threshold is necessary but also that the gametes need to be mature. Compared with deeper waters, at 2.5 m there was less food, which is necessary for the gametes to ripen.

At 2.5 m from early May until September 22, the seawater temperature was always more than 16.0[degrees]C, but spawning did not take place until June 10. The faster growth and the high GCI recorded at 2.5 m in early spring are probably related to warmer temperatures; however, spawning took place later when the seawater reached temperatures greater than 16.5[degrees]C. Warmer temperatures but lower food availability can be associated with faster gonad growth but slower maturation. Therefore, gametes are not ripe enough to be spawned, regardless of reaching the appropriate temperature. At 12.5 m and 7.5 m, where there is greater food availability, the gametes mature earlier, and a temperature of 16[degrees]C is enough to trigger spawning. The spawning cessation at 7.5 m and 12.5 m in the middle of July is related to a small decrease in temperature to less than 16.0[degrees]C at 7.5 m (14.4[degrees]C) and 12.5 m (14.3[degrees]C), but not at 2.5 m (17.4[degrees]C). Afterward, there was a significant GCI recovery at 7.5 m and 12.5 m, but not at 2.5 m.

The 2 species have different temperature requirements; C. varia requires a minimum of 16[degrees]C for spawning, which stops when less than this value, whereas A. opercularis requires 14.0-14.5[degrees]C to trigger spawning. Gonadic growth is accelerated by warmer temperatures, as can be seen in the first gonad growth in both species, but temperature as a single factor does not indicate gamete maturation despite faster growth, because food is required for gametes to mature. According to our results, we conclude that temperature, in the tolerance range for each species, affects both the growth rate of the gonad and somatic tissues, and triggers spawning, whereas food availability influences growth and the amount of energy stored, and allows the gametes to mature.

Comparison Between Species

The species we studied have different reproductive patterns (gonad and reserve storage organ growth, breeding season timing) and environmental requirements--mainly, temperature. The gonad of A. opercularis not only is active for a longer period of the year, having a very short resting period in middle summer, (which is the opposite from C. varia, which has a resting period that ranges from autumn to the end of winter) but also reaches higher values with maxima values 2-fold those recorded in C. varia.

The DGCI of C. varia displays high values in a single cycle during a short period between July and August, with the maxima being almost twice that attained by DGCI of A. opercularis. The maxima values are reached in summer just in the period, when A. opercularis displays minimal values; A. opercularis presents a more complex evolution, which is probably related to the conservative pattern and it is more affected by small differences in environmental conditions, with maxima values in spring and autumn.

The evolution of the MCI follows the same pattern as the DGCI in the case of C. varia, maxima values being recorded at the end of summer. As is the case with the DGCI, the evolution of the MCI does not appear to be affected by the differences in the environmental conditions observed at the experimental depths tested. This is not the case in A. opercularis, where food and temperature were related to differences in the index evolution. In this species, the MCI increases for a longer period, reaching higher values by the end of November before being employed for fueling gametogenesis.

In the case of C. varia, after fueling the start of gametogenesis, probably triggered by the photoperiod (Louro et al. 2005), and when gonad maturation has been reached, the MCI and DGCI take advantage of the favorable environmental conditions (greater level of available food and temperature) for a rapid, single, and short period of growth and storage of reserves, according its opportunistic condition.

CONCLUSIONS

This work provides useful information both for a better understanding of the requirements of the species and for optimizing aquaculture. It has been shown that small environmental changes associated with the depth where the scallops are grown lead to significant changes in the general trends of the reproductive and reserve storage organs. A general conclusion of our study is that growing scallops at depths between 7.5 m and 12.5 m provides better results than growing them at 2.5 m, and both significantly larger scallops (C. varia) and scallops with more meat (A. opercularis) could be obtained by to the harvest date. Moreover, although low salinity values were not recorded in the upper layer, suspension culture of scallops in shallow water can be risky during rainy years.

This study also provides some information about conditioning. Keeping A. opercularis under 14[degrees]C and C. varia under 16[degrees]C, and providing sufficient food, can result in the production of abundant gametes that are released easily when the temperature is increased slightly, at least in the case of C. varia, as A. opercularis has proved to be a difficult species to make spawn under laboratory conditions (Le Pennec 1982, Beaumont & Hall 1999, De la Roche et al. 2003).

The case of C. varia is especially interesting because, in natural conditions, most of the spat settle on collectors in the middle of spring and at the beginning of summer at the same time as the settlement of the starfish Asterias rubens, which eliminates all the spat. The settlement originated by the second spawning, which occurs at the end of summer, is hardly preyed on by starfish, because by this date starfish settlement has finished. In this sense, the gonad can be managed by growing black scallops in deeper waters to produce a large second spawning after starfish settlement.

ACKNOWLEDGMENTS

We thank the Instituto Tecnoloxico para o Control do Medio Marino de Galicia for providing the environmental data on salinity, temperature, and chlorophyll a.

LITERATURE CITED

Ansell, A. D. 1974. Seasonal changes in biochemical composition of the bivalve Chlamys septemradiata from the Clyde Sea Area. Mar. Biol. 25:85-49.

Barber, B. J. & N. J. Blake. 1981. Energy storage and utilization in relation to gametogenesis in Argopecten irradians concentricus (Say). J. Exp. Mar. Biol. Ecol. 52:121-134.

Barber, B. J. & N. J. Blake. 1983. Growth and reproduction of the bay scallop, Argopecten irradians (Lamarck), at its southern distributional limit. J. Exp. Mar. Biol. Ecol. 66:247-256.

Barber, B. J., R. Getchell, S. Shumway & D. Schick. 1988. Reduced fecundity in a deep-water population of the giant scallop Placopecten magellanicus in the Gulf of Maine, USA. Mar. Ecol. Prog. Ser. 42:207-212.

Bayne, B. L. 1976. Aspects of reproduction in bivalve molluscs. In: M. Wiley, editor. Estuarine processes, vol. 1. Uses, stresses and adaptation to the estuary. New York: Academic Press. pp. 432-448.

Beaumont, A. & V. Hall. 1999. Getting the queen to spawn: experiments with Aequipecten opercularis. Presented at the 12th International Pectinid Workshop. Norway, May 5-11.

Brea, J. 1986. Variaciones energeticas estacionales en ta composicion bioquimica de Pecten ziczac (Linnaeus, 1750), en relacion con el metabolismo energetico, reproduccion y crecimiento. Tesis de licenciatura. Escuela de Ciencias, Universidad de Oriente, Cumana (Venezuela). 75 pp.

Broom, M. J. & J. Mason. 1978. Growth and spawning in the pectinid Chlamys opercularis in relation to temperature and phytoplankton concentration. Mar. Biol. 47:277-285.

Burnell, G. M. (1983). Growth and reproduction of the variegated scallop Chlamys varia (L.) on the west coast of Ireland. Thesis. University College Galway. 295 pp.

Campos, M. J., G. Roman, J. Cano & C. P. Acosta. 2001. Growth and reproduction of the queen scallop, Aequipecten opercularis, in suspended culture in Galicia (NW Spain). Presented at the 13th International Pectinid Workshop. Coquimbo, Chile, April 18-24.

De la Roche, J. P., A. Louro & G. Roman. (2003). Spawning induction of the queen scallop Aequipecten opercularis in the hatchery. Presented at the 14th International Pectinid Workshop. St. Petersburg, FL; April 23-29.

Gabbot, P. A. 1975. Storage cycles in marine bivalve molluscs: a hypothesis concerning the relationship between glycogen metabolism and gametogenesis. In: H. Barnes, editor. Proceedings of the 9th European Marine Biological Symposium. Aberdeen: Aberdeen University Press. pp. 191-211.

Hart, D. R. & A. S. Chute. 2004. Essential fish habitat source document: sea scallop, Placopecten magellanicus, life history and habitat characteristics, 2nd edition. NOAA technical memorandum NMFS NE189. Woods Hole, MA: U.S. Department of Commerce, USA. 21 pp.

Hart, D. R. & A. S. Chute. 2009. Estimating von Bertalanffy growth parameters from growth increment data using a linear mixed-effects model, with an application to the sea scallop Placopecten magellanicus. ICES J. Mar. Sci. 66:2165-2175.

Hart, D. R. & P. J. Rago. 2006. Long-term dynamics of U.S. Atlantic sea scallop Placopecten magellanicus populations. N. Am. J. Fish. Manage. 26:490-501.

Lai, H. L. & T. E. Helser. 2004. Linear mixed-effects models for length weight relationships. Fish. Res. 70:377-387.

Le Pennec, M. 1982. L'alevage experimental de Chlamys opercularis (L.) (Bivalvia, Pectinidae). Vie marine 4:29-36.

Louro, A., J. P. De la Roche, J. L. Sanchez, A. Silva, P. Martinez, M. L. Perez-Paralle, I. Martinez & G. Roman. 2005. The effect of photoperiod on the conditioning of the black scallop Chlamys varia. I: gonadal development. Presented at the 15th International Pectinid Workshop. Mooloolaba, Australia; April 20-26.

Lubet, P. 1959. Recherches sur le cycle sexuel et l'emission des gametes chez les mytilides et les pectinides. Thesis. Rev. Tray. Off. Peches Marit. 23:387-548.

Lucas, A. 1965. Recherche sur la sexualite des mollusques bivalves. Thesis, Faculte des Sciences de Rennes. 136 pp.

Luna-Gonzalez, A. 1997. Ciclo reproductivo de la almeja catarina Argopecten ventricosus (Sowerby II, 1842), cultivada en la rada del Puerto de Pichilingue, B. C. S. y su relacion con el medio. Master's thesis, Universidad Autonoma de Baja California Sur. 74 pp.

MacDonald, B. A. & R. J. Thompson. 1985. Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus: I. Growth rates of shell and somatic tissue. Mar. Ecol. Prog. Ser. 25:279-294.

MacDonald, B. A. & R. J. Thompson. 1986. Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus: 3. Physiological ecology, the gametogenic cycle and scope for growth. Mar. Biol. 93:37-48.

MacDonald, B. A. & R. J. Thompson. 1988. Intraspecific variation in growth and reproduction in latitudinally differentiated populations of the giant scallop Placopecten magellanicus (Gmelin). Biol. Bull. 175:361-371.

Mason, J. 1957. The age and growth of the scallop, Pecten maximus (L), in Manx waters. J. Mar. Biol. Assoc. UK 36:473-492.

McLusky, D. S. 1973. The effect of temperature on oxygen consumption and filtration rate of Chlamys (Aequipecten) opercularis (L.) (Bivalvia). Ophelia 10:141-154.

Parada, J. M., M. J. Cancelo, A. Fernandez & A. Guerra. 1993. Comportamiento reproductivo de la zamburina (Chlamys varia L.), cultivada en batea en Galicia (NO de Espana). In: A. Cervino, A. Landin, A. de Coo, A. Guerra & M. Torre, (eds.). Actas IV Congreso Nacional de Acuicultura. Santiago de Compostela-A Coruna: Conselleria de Pesca, Marisqueo e Acuicultura, Xunta de Galicia. pp. 317-322.

Pazos, A. J., G. Roman, C. P. Acosta, M. Abad & J. J. Sanchez. 1997. Seasonal changes in condition and biochemical composition of the scallop Pecten maximus L. from suspended culture in the Ria de Arousa (Galicia, NW Spain) in relation to environmental conditions. J. Exp. Mar. Biol. Ecol. 211:169-193.

Paul, J. D. 1980a. Salinity-temperature relationships in the queen scallop Chlamys opercularis. Mar. Biol. 56:295-300.

Paul, J. D. 1980b. Upper temperature tolerance and the effect of temperature on byssus attachment in the queen scallop, Chlamys opercularis (L.). J. Exp. Mar. Biol. Ecol. 46:41-50.

Posgay, J. A. 1979. Depth as a factor affecting the growth rate of the sea scallop. ICES document CM 1979/K: 27.5 pp.

Roman, G. & C. Acosta. 1990. Cultivo de vieira en batea. II: Reproduccion. In: Actas III Congreso Nacional de Acuicultura. A. Landin & A. Cervino, (eds). Conselleria de PEsca, Marisqueo e Acuicultura, Xunta de Galicia, Santiago de COmpostela, A Coruna (Spain). pp. 461-466.

Roman, G., M. J. Campos, C. P. Acosta & J. Cano. 1999. Growth of the queen scallop (Aequipecten opercularis) in suspended culture: influence of density and depth. Aquaculture 178:43-62.

Roman, G., G. Martinez, O. Garcia & L. Freites. (2002). Reproduccion. In: A. N. Maeda-Martinez, editor. Los moluscos pectinidos de Iberoamerica: ciencia y acuicultura. Editorial Limusa, S.A. de C.V. Mexico, Mexico D.F. pp. 27-59.

Shafee, M. S. 1981. Seasonal changes in the biochemical composition and caloric content of the black scallop Chlamys varia (L.) from Lanveoc, Bay of Brest. Oceanol. Acta 4:331-341.

Schick, D. F., S. E. Shumway & M. A. Hunter. 1988. A comparison of growth rate between shallow water and deep water populations of scallops, Placopecten magellanicus (Gmelin, 1791), in the Gulf of Maine. Am. Malacol. Bull. 6:1-8.

Schmitzer, A. C., W. D. DuPaut & J. E. Kirkley. 1991. Gametogenic cycle of sea scallops (Placopecten magellanicus (Gmelin, 1791)) in the mid-Atlantic Bight. J. Shellfish Res. 10:221-228.

Skreslet, S. & E. Brun. 1969. On the reproduction of Chlamys islandica (O. F. Muller) and its relation to depth and temperature. Astarte 2:1-6.

Smith, S. J., E. L. Kenchington, M. J. Lundy, G. Robert & D. Roddick. 2001. Spatially specific growth rates for sea scallops (Placopecten magellanicus). In: G. H. Kruse, N. Bez, A. Booth, M. W. Dorn, S. Hills, R. N. Lipcius, D. Pelletier, C. Roy, S. J. Smith & D. Witherell, editors. Spatial processes and management of marine populations. AK-SG-01-02. Fairbanks: University of Alaska Sea Grant. pp. 211-231.

PAULA IGLESIAS, ANGELES LOURO AND GUILLERMO ROMAN *

Instituto Espanol de Oceanografia, Centro Oceanografico de A Coruna, PO Box 130, 15080 A Coruna, Spain

* Corresponding author. E-mail: guillermo.roman@co.ieo.es

DOI: 10.2983/035.031.0311
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