Reproductive cycle of the cockle Cerastoderma edule (linnaeus 1758) in the Ria de Vigo (Galicia, Northwest Spain).
Article Type: Report
Subject: Clams (Sexual behavior)
Spawning (Research)
Authors: Martinez-Castro, C.
Vazquez, E.
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: 0913030 Clams NAICS Code: 114112 Shellfish Fishing SIC Code: 0913 Shellfish
Geographic: Geographic Scope: Spain Geographic Code: 4EUSP Spain
Accession Number: 303011399
Full Text: ABSTRACT The reproductive cycle of the cockle Cerastoderma edule was studied by histological techniques and observation of changes in the condition index during three consecutive years in the Ria de Vigo (Northwest Iberian Peninsula). The onset of gametogenesis took place at the end of the summer (September to October), progressed throughout the winter, and the mature stage was finally reached in spring. The first spawning occurred in April and May and, after gonad restoration, another spawning episode took place in May and June. During the summer (July and August), most of the population showed signs of gonad exhaustion, although a less-intensive spawning event was observed at the end of summer and beginning of autumn. This second episode coincided with a phytoplankton bloom, which acted as a stimulus for spawning. Although a simple measure, the condition index proved to be a good indicator of the gonadal cycle, because it reflected adequately the reserve accumulation during gametogenesis, maximum maturity, and gamete emission. The useful information obtained from this study can he applied in shellfishery management.

KEY WORDS: Cerastoderma edule, cockle, bivalve, reproduction, condition index, shellfishery management

INTRODUCTION

The Galician coast (Northwest Iberian Peninsula) is characterized by the presence of several coastal inlets, known as rias. These inlets are highly productive environments that have supported important fisheries for centuries. Apart from the mussel Mytilus galloprovincialis (Lamarck 1819), which is cultured on hanging ropes and is the most important marine resource in the region, the shellfish fishery has targeted predominantly the cockle (Cerastoderma edule Linnaeus 1758) and several species of clam such as Ruditapes philippinarum (Adams and Reeve 1850) and Venerupis pullastra (Montagu 1803). Cockle fisheries were the most productive bivalve fisheries in Galicia in 2009, with a net product weight of 3,255 t, with a commercial value of more than (14 million (Xunta de Galicia 2010).

Knowledge of the reproductive cycle of economically important marine bivalves is essential for population management so that harvesting practices such as closed seasons can be established. Although many studies have been made of the most important species, the gametogenic cycle varies between populations in response to interactions with external factors (e.g., temperature, salinity, light, availability of food, parasitic infestations) and internal factors (genetics). Reproduction of C. edule has been studied extensively. Thus, in its northern area of distribution, the species has shown a rapid maturation phase in spring, followed by a short spawning period in May through July (Rygg 1970, Boyden 1971, Hancock & Franklin 1972, Seed & Brown 1977, Newell & Bayne 1980, Yankson 1986). On the other hand, in southern populations, the onset of gametogenesis takes place in autumn, and spawning occurs in March and April (Deltreil & His 1972, Gonzalez & Perez Camacho 1984, Mejuto 1984a, Mejuto 1984b, Saavedra 1984, Fernandez Castro et al. 1989, Navarro et al. 1989, Guillou et al. 1992, Iglesias 2006). This gradient has led some authors to attempt to show a direct influence of latitude, as a covariate of temperature, on the reproductive cycle. However, many exceptions to this general assumption have been found for a wide range of scales. Guillou et al. (1990) observed a high degree of variability in the reproductive pattern of cockles along the Atlantic French Coast, not linked to the latitudinal gradient. On a smaller scale, Boyden (1971) found that cockles from the lowest intertidal zones matured earlier than those from higher areas. The same cockle population may even follow different reproductive strategies in consecutive years, in response to several environmental factors (Yankson 1986, Navarro et al. 1989).

The marketable value of the cockle is related to the quality and quantity of the meat, which are both determined by the reproductive stage of the animal. An understanding of the effects of local environmental conditions on gametogenesis in C. edule is therefore considered essential for planning cockle harvesting practices. However, studies of invertebrate reproduction are relatively expensive in terms of time, effort, and money, and often involve a considerable amount of intensive field and laboratory work, including examination of thin sections by microscopy. The development of simpler techniques for determining the reproductive stage of cockle populations would thus be advantageous.

Condition indices are regarded as useful measures of the physiological state of an organism under given environmental conditions. Two types of such indices can be distinguished: those determined over a period of time in a given population (dynamic) and those determined at a single point in time (static) (Lucas & Beninger 1985). Dynamic condition indices are calculated as the difference in the values of two parameters measured at a chosen time interval. Some examples are the net growth efficiency and the scope for growth. On the other hand, static condition indices are calculated as a ratio between two physiologically significant variables, such as wet weight: dry weight ratio, RNA:DNA ratio, and glycogen, protein, or lipid:total weight ratio. In bivalves, the presence of a mineral shell, which represents cumulative growth, and a body consisting of tissues that vary depending on the current sexual and metabolic activity of the organism, greatly facilitates estimates of static condition indices, and many can be defined on the basis of the variables involved (Lucas & Beninger 1985, Crosby & Gale 1990). The dry flesh weight:dry shell weight ratio, defined by Walne (1976) has been used widely to describe the sexual cycle of several bivalve species, including C. edule (Beninger & Lucas 1984, Fernandez Castro et al. 1989, Guillou et al. 1990, Guillou & Tartu 1992, Guillou et al. 1992, Ruiz et al. 1992, Cano et al. 1997, Gaspar & Monteiro 1998, Ojea et al. 2002, Boscolo et al. 2003, Liu et al. 2008). The latter ratio is calculated easily because of the nature of the measurements involved, and it also provides meaningful information about the sexual maturity of the population under study (Lucas & Beninger 1985). This index has also been used as an indicator of the reproductive output of C. edule because it provides a quantitative measure of gametogenic activity (Guillou et al. 1992).

The current study describes the reproductive cycle of C. edule in 2 sandflats in the Ria de Vigo (Northwest Iberian Peninsula) in relation to environmental factors. The main objectives were: (1) to establish the pattern of gametogenesis; (2) to study the influence of temperature, salinity, and concentration of chlorophyll a (Chl a) on the reproductive cycle; and (3) to correlate the condition index with the gametogenetic cycle to use the former as a simple tool in shellfishery management.

MATERIALS AND METHODS

Area of Study and Sampling

Samples were collected between December 2001 and December 2004 in the 2 intertidal sandflats with the largest cockle production of the Ria de Vigo: A Xunqueira and Punta do Cabo (Fig. 1). Sampling was carried out at monthly intervals between October and March, and at fortnightly intervals between April and September (i.e., during periods when cockles are thought to be sexually active).

The Ria de Vigo is the southernmost of the 4 Galician Rias Baixas (Fig. 1). It has a characteristic V shape, with its central axis lying in a southwest northeast direction. It occupies an area of 176 [km.sup.2] and the water is generally less than 50 m deep. After the Rande Strait, the narrowest part of the ria, it widens to form a well-differentiated, very shallow basin--the Ensenada de San SimSn (Nombela et al. 1995, Evans et al. 2003)--where most of the river discharge occurs (Perez-Arlucea et al. 2005, Santos-Echeandia et al. 2008).

[FIGURE 1 OMITTED]

A Xunqueira is a large intertidal sandflat (230.840 [m.sup.2]) located in the northern margin in the central part of the ria. Punta do Cabo is a sandy tongue situated close to the San Sim6n Island, in the Ensenada de San Sim6n. It is a smaller intertidal flat (127.426 [m.sup.2]) with muddy sand in the lower intertidal zone and coarser sand in the upper zone (Fig. 1).

Histological Analysis

For histological analysis, 15 cockles of lengths ranging from 20-31 mm were collected at each sampling time and were maintained in filtered seawater for 24 h prior to histological processing to allow the animals to expel sand particles from the digestive tract. The cockles used were always larger than 20 mm to make sure they were sexually mature (C. edule's first maturation size in the Galician rias is 15-19 mm (Mejuto 1984b, Perez Camacho & Roman 1984)). Because the gonad is a diffuse tissue, a piece of tissue ca. 8 mm was dissected from the foot and processed routinely for histology: fixed in Baker's formaldehyde for 24 h, embedded immediately in paraffin, sectioned at 5 [micro]m, and stained with hematoxylin-eosin. The stages of gonad development were scored according to the scale proposed by Iglesias (2006) as follows:

Sexual resting (stage 0): Follicles are scarce, isolated, and small. Sexes are difficult to distinguish at this stage (Fig. 2A).

Initiation of gametogenesis (stage 1): Follicles become evident, increasing in size and number. Their walls are full of germ cells--oogonias and previtellogenic oocytes in females (Fig. 2B) and spermatogonias and primary spermatocytes in males (Fig. 3A).

Advaneed gametogenesis (stage 2): Follicles occupy most of the visceral mass, and germinal cells are present at all stages of gametogenesis. In females, free oocytes in the lumen and immature oocytes attached to the basal membrane are observed at different stages of vitellogenesis (Fig. 2C). In males, spermatogonia, spermatocytes, spermatids, and some radially arranged spermatozoa are present (Fig. 3B).

Ripe (stage 3): Polygonal follicles are almost full of ripe gametes. In females, ripe oocytes, free in the lumen, are polygonal as a result of packing (Fig. 2D). In males, spermatozoa are distributed radially with the tails pointing toward the center of the follicle (Fig. 3C).

Post-spawning (stage 4A): As a result of the partial release of the gamete, pressure inside the follicle decreases. In females, empty spaces in the follicular lumen are observed, although some ripe oocytes are present (Fig. 2E). In males, spermatozoa lose their radial arrangement and follicles are partly empty (Fig. 3D).

Gonad restoration (stage 4B): After spawning, a new gametogenic cycle begins in the follicles and new germ cells appear in the follicle walls. This stage is similar to advanced gametogenesis, but follicles are larger and new germ cells coexist with ripe gametes. In females, oogonias in division in the follicle walls, numerous previtellogenic oocytes, and scarce free ripe oocytes in the lumen are observed (Fig. 2F). In males, the number of spermatocytes increases again, in contrast to the small number of spermatozoa (Fig. 3E).

Resorption (stage 5): Cytolysis begins in the gonad (phagocytic cells are common) and follicles become very small and practically empty. In females, some oocytes, showing clear signs of cytolysis, are present, and in males, some spermatozoa remain (Figs. 2G and 3F).

[FIGURE 2 OMITTED]

Condition Index

To study the changes in the condition index, at least 20 cockles ranging from 21-25 mm in length were caught and measured to the nearest millimeter. The soft parts were then extracted and rinsed gently with distilled water. The flesh and the valves were dried in an oven at 60[degrees]C for 48 h, and weighed to the nearest milligram to obtain the flesh dry weight (FDW) and the valve dry weight (VDW). The condition index (CI) proposed by Walne (1976), (FDW/VDW) x [10.sup.3], was applied. Changes in weight were related to somatic growth or variations in the size of the specimens between successive sampling. To minimize this effect, only cockles ranging from 21-25 cm in length were analyzed. However, the numbers of cockles in this size class obtained in July and September 2002, and between November 2003 and March 2004 at the A Xunqueira site, and in January and February 2003, and in March and July 2004 at the Punta do Cabo site were not sufficient for calculation of the CI.

Environmental Variables

To evaluate the possible influence of environmental factors on the cycle, temperature, salinity, and concentration of Chl a were recorded weekly in the water column at a depth of 5 m at 2 sites used in the monitoring program carried out by the Instituto Tecnoldxico para o Control do Medio Marino de Galicia (INTECMAR-Xunta de Galicia), close to the sandflats under study (V2-Moafia, 42[degrees]16'00" N, 08[degrees]43' 10" W, close to the A Xunqueira sandflat; and V3-Rande, 42[degrees] 17' 30" N, 08[degrees]38'48" W, close to the Punta do Cabo sandflat; Fig. 1). Temperature and salinity were measured with a CTD system, and the concentration of Chl a was determined by spectrofluorometry.

[FIGURE 3 OMITTED]

Rainfall data recorded at 2 stations close to the sampled sandflats were provided by the Agencia Estatal de Meteorologia (AEMET).

Statistical Analysis

To test possible deviations from the 1:1 ratio of the proportion of males:females at each study site, chi-square analysis was conducted on data from all specimens analyzed by histological methods (302 in A Xunqueira and 314 in Punta do Cabo).

The CI data were presented using the mean and the SD as estimators of the central trend of the sample. According to Grant and Tyler (1983), SD is useful in this type of plot because it reflects the synchronicity of the population.

Interannual and interlocation differences in CI, water temperature, salinity, and concentration of Chl a were analyzed by 1-way ANOVA, with SPSS. To meet assumptions of homogeneity of variance, the CI data were transformed by log(x). The Tukey post hoc test was applied when the assumptions of homogeneity of variance assumption were met, and the Games-Howell test was used when the assumptions were not met.

Cross-correlations among CI, seawater temperature, and concentrations of Chl a were calculated to assess the influence of the environmental factors on the reproductive cycle.

RESULTS

Histological Analysis

Of the 302 individuals sampled at the A Xunqueira site, 34.4% were males, 49.7% were females, and 15.9% were of undetermined sex. The number of females was therefore significantly higher than the number of males (chi-square = 8.331, df = 1). However, at the Punta do Cabo site, where 314 individuals were analyzed, the male:female ratio did not differ significantly from 1:1 (chi-square = 1.883, df = 1), and was 41.1% male, 48.4% female, and 10.5% undetermined.

Development of the gonadal cycle was basically the same in both sandflats (Fig. 4). Gametogenesis began at the end of the summer (September and October), when most individuals were at stage 1. Gametogenesis progressed during the winter (stage 2), and the mature stage (stage 3) was finally reached during the spring. The first spawning occurred in April and May and, after gonad restoration (stage 4B), another spawning episode took place in May and June. During the summer (July and August), most of the population showed signs of gonad exhaustion (stage 5), although less-intensive spawning was observed at the end of summer/beginning of autumn, revealed by a large number of individuals at the postspawning stage (50% of individuals in stage 4A in September 2003 at Punta do Cabo). After a short sexual resting stage (end of August through September), a new cycle began.

[FIGURE 4 OMITTED]

Condition Index

A comparison between histological stages and CI in both sandflats revealed that the maximum CI values occurred when most individuals reached maturity (stage 3) (Fig. 4). Moreover, sharp decreases in CI values coincided with the times when most individuals were at the postspawning stage (stage 4A) or the gonad restoration stage (stage 4B). However, the minimum CI values did not coincide with the sexual resting stage, but were reached in January and February, when the populations were at the stage of advanced gametogenesis (stage 2). Although the lowest CI values did not correspond to the sexual resting stage, changes in CI have been found to be a good indicator of the reproductive cycle because they indicate accurately the accumulation of reserves for gametogenesis, the mature stage, and spawning.

In both sandflats in the 3 y studied, changes in CI were minimal in February, with a sharp increase in March before reaching maximum values between April and June (Figs. 5A and 6A). Another peak was observed in October, with values then decreasing to the low winter values. In 2002, the pattern was slightly different in both sandflats, with unusually high values in December 2001 and a slight increase at the end of winter. Moreover, the maximum CI values occurred later, at the end of May through June.

Significant interannual differences in the CI were observed for both sandftats. The CI of cockles from the A Xunqueira site was significantly higher in 2004 than in 2002 and 2003 (ANOVA, P [less than or equal to] 0.001), whereas for cockles from the Punta do Cabo site, CI was significantly higher in 2003 (ANOVA, P [less than or equal to] 0.001) than in the other years. Moreover, the CI of cockles from the Punta do Cabo site was significantly higher than the CI of those from the A Xunqueira site (ANOVA, P [less than or equal to] 0.001), except when values corresponding to A Xunqueira in 2004 and Punta do Cabo in 2003 were compared, which did not reveal any significant differences (ANOVA, P = 0.860).

[FIGURE 5 OMITTED]

Environmental Factors

Temperature

During the sampling period, the lowest temperature was recorded between December and March, coinciding with the minimum CI values at both sites (Figs. 5B and 6B). From March onward, the temperature increased sharply (4-7[degrees]C), as did the CI values. The highest temperature was recorded in July and August at both sites, except in 2002 when the highest temperature was recorded between September and October. This shift was also reflected in the CI, as the highest value was reached later in both sandflats.

The good correlation between temperature and CI was corroborated by the results of cross-correlation analysis (Fig. 7A, B). At the A Xunqueira site, the maximum correlation was obtained with a time lag of-1 mo and 0 mo (r = 0.614 and r = 0.496, respectively; P [less than or equal to] 0.05). In other words, the CI peak was reached 1 mo earlier or at the same time as the maximum temperature (Fig. 7A). However, in the Punta do Cabo site, no significant correlation was observed (Fig. 7B).

There were no significant interannual differences in temperature during the study period (ANOVA, P = 0.403 for the site close to A Xunqueira and P = 0.683 for the site close to Punta do Cabo). No significant differences between sampling stations were observed (ANOVA, P = 0.549).

Salinity

Salinity remained constant (ca. 35) between March and October at both sites (Figs. 5C and 6C). However, several decreases in salinity took place during the winter as a result of rainfall. In January 2003, salinity values of 26 and 23 were recorded at the sites close to A Xunqueira and Punta do Cabo, respectively. When comparing annual mean values, the salinity in 2002 and 2003 was significantly lower than in 2004 at V3-Moafia (Games-Howell, P [less than or equal to] 0.05 and P [less than or equal to] 0.001), whereas at V2-Rande in 2003, it was only significantly lower than in 2004 (Games-Howell, P [less than or equal to] 0.01). Moreover, salinity was significantly lower at V2-Rande, located in the inner part of the ria, where most of the river discharge occurs, than at V3-Moafia (ANOVA, P [less than or equal to] 0.001).

[FIGURE 6 OMITTED]

Chlorophyll a

The highest concentrations of Chl a were recorded between May and October through November at both sites, coinciding with an increase in surface temperature (Figs. 5D and 6D). During winter, the concentration of Chl a was relatively low (ca. 0.3 [micro]g/L). Because gametogenesis is an energy-dependent process, a cross-correlation between the concentration of Chl a and CI was carried out for both sandflats (Fig. 7C, D). A significant correlation was observed only for the A Xunqueira site, with a time lag of 0 (r = 0.631, P [less than or equal to] 0.05), which reveals that the maximum CI values coincide with the maximum food availability.

The concentration of Chl a was not significantly different among years or between sampling sites (ANOVA, P > 0.05), although the maximum concentrations of Chl a at the V2-Rande site were higher than those at the V3-Moana site.

DISCUSSION

The cockle C. edule is a gonochoric species and, although hermaphrodites or even sex reversals have been found occasionally (Kingston 1974, Fernandez Castro et al. 1989), none were identified in this study. The sex ratio for cockle populations is considered to be 1:1, although several exceptions--in which the number of females was higher--have also been observed (Boyden 1971, Mejuto 1984a, Mejuto 1984b, Desprez et al. 1987, Fernandez Castro et al. 1989), probably as a result of the difficulty in determining sex at the beginning of gametogenesis and at the spawned-out stage in males (Boyden 1971). However, in our case, the significantly greater number of females found in the A Xunqueira population may not be relevant, given the greater number of undifferentiated individuals.

[FIGURE 7 OMITTED]

Because of the importance of C. edule as a natural resource, the reproductive cycle of the species in the Galician rias was established previously by analysis of gonad smears (Figueras 1957, Gonzalez & Perez Camacho 1984, Mejuto 1984a, Mejuto 1984b, Perez Camacho & Roman 1984). However, this method is much less accurate than histological methods because only the presence of ripe oocytes can be discriminated, which does not necessarily indicate forthcoming spawning, because oocytes can be stored in the gonad for long periods. Moreover, smears do not reveal accurately the onset of gametogenesis or gonad restoration processes, which are very common in other bivalve species (Crassostrea gigas (Ruiz et al. 1992), Mytilus galloprovincialis (Villalba 1995), Ensis arcuatus (Darriba et al. 2004), and Tapes decussatus (Rodriguez-Moscoso & Arnaiz 1998)). An exhaustive histological analysis was conducted recently as part of a pathological study in 3 northern Galician sandflats, which revealed latitudinal-related differences in the reproductive pattern (Iglesias 2006).

Given the importance of the reproductive stage with regard to the market value of cockles and the observed differences in the reproductive cycle, a simple method of determining the reproductive stage would be a useful tool in cockle fishery management. The CI used in the current study has been confirmed as a precise indicator of maximum gonad ripeness and spawning periods, as the values were correlated closely with the gonad state identified by histological methods. In both sandflats, the increase in the CI values coincided with most individuals being at an advanced stage of gametogenesis, the maximum CI values occurred when the cockles were mature, and the sharp decreases corresponded to a high percentage of specimens at the postspawning stage, as a consequence of weight loss resulting from gamete release. Conversely, the minimum CI values (recorded in January and February) did not coincide with the sexual resting period (August and September). Similar results have been found for this species on the French Atlantic coast (Fernandez Castro et al. 1989, Guillou et al. 1990, Guillou & Tartu 1992, Guillou et al. 1992). Because the index considers all the meat (somatic and gonadal tissues), variations may be influenced by other factors not directly related to gonad development, such as somatic growth and storage of reserves, which usually occur during the summer (Larretxea 1995). Some authors have indicated that consideration of all the flesh in the calculation of CIs is not correct (Aracena et al. 2003, Darriba et al. 2004). However, in cockles in which gonad is diffuse, the CI used here provides an accurate description of sexual development, so it will be extremely useful as a management tool in cockle fisheries in which the reproductive cycle has not yet been studied.

The reproductive pattern described in the current study (initiation of gametogenesis in autumn, 2 consecutive spawning events in March and April and May and June, and a short gonadal resting stage at the end of summer/beginning of autumn) is similar to that found by Iglesias (2006) in other Galician sandflats. Nonetheless, the later spawning period observed in autumn in the Ria de Vigo was not detected in those northern localities. Similar latitudinal-related variability has been observed along the European Atlantic coast (Rygg 1970, Boyden 1971, Hancock & Franklin 1972, Seed & Brown 1977, Newell & Bayne 1980, Gonzalez & Perez Camacho 1984, Mejuto 1984a, Mejuto 1984b, Saavedra 1984, Iglesias 2006), according to the general assumption that in species with a wide geographical distribution, spawning occurs earlier and lasts longer in the southern populations than in the northern populations, mainly as a result of temperature-related differences (Newell et al. 1982). Traditionally, water temperature has been considered the key environmental factor that controls the reproductive cycles of marine invertebrates (Newell et al. 1982), and temperature thresholds at which gametogenesis is triggered and spawning is induced have even been reported for several bivalve species, including C. edule (Gimazane 1972, Gimazane & Lubet 1972, Boyden 1971). However, reports of different temperatures at which the spawning occurs have led some authors to suggest a sudden increase in temperature, rather than the absolute temperature, as a stimulus for spawning (Guillou et al. 1990, Ducrotoy et al. 1991, Guillou et al. 1992). In the current study, the simultaneous increase in temperature and CI values, together with the results obtained in the cross-correlation analysis, reinforce this assumption.

At the same time, water temperature has been indicated as the determining factor in the interannual and spatial variability in cockle CI values (a quantitative indicator of individual fecundity) recorded along the European Atlantic coast, (Guillou et al. 1990, Guillou & Tartu 1992, Guillou et al. 1992). In general, greater temperatures have been associated with a greater reproductive output because they favor gonad development and increase gamete quality, which in some cases may lead to greater recruitment (Menesguen & Dreves 1987, Guillou et al. 1992). In the Ria de Vigo, CI values varied to the same degree (Gonzalez & Perez Camacho 1984, Perez Camacho & Roman 1984, Fernandez Castro et al., Guillou et al. 1990, Guillou & Tartu 1992, Guillou et al. 1992), although temperature was not the determining factor because no significant differences in either spatial or interannual variability were observed during the study period. Spatial variability in CI values followed the pattern observed by Gonzalez and Perez Camacho (1984) in another Galician ria, where--as in the Ria de Vigo--greater CI values were recorded in the inner zone, where salinity is lower. Although C. edule populations tolerate a relatively wide range of salinity (10-35[per thousand]), the optimum salinity is 25[per thousand] (Ysebaert et al. 2002), which is closer to the values registered at the V2-Rande site. Thus, populations from Punta do Cabo, a more favorable environment, would suffer less stress and would be able to increase the energy destined for reproduction, showing greater CI values. On the other hand, sharp decreases in salinity may have negative effects on reproduction, delaying gametogenesis and even spawning (Iglesias 2006). This delay would explain the abnormal pattern observed in both sandflats in 2002, with unusually high CI values in the winter and a minor increase at the beginning of the spring, just after an extraordinarily rainy winter (2000 to 2001) that resulted in high mortality rates in cockle populations (Molares et al. 2008).

Food availability was considered to be another important factor affecting the reproductive cycle of bivalves, and several studies have even indicated this as the main determining factor, rather than temperature (Newell et al. 1982, Navarro et al. 1989, Ruiz et al. 1992). Navarro et al. (1989) described a cockle population in which different reproductive patterns occurred in 2 consecutive years, under the same temperature regime, simply as a result of the prior feeding conditions. When the food available in the summer was sufficient to meet the energy requirements associated with gonadal development, gametogenesis occurred in winter. However, gametogenesis was delayed until spring when food was scarce during the previous summer.

Food does not appear to be a limiting factor in the Ria de Vigo, as revealed by the high concentrations of Chl a. Although the concentrations of Chl a did not vary significantly between sampling sites, the peaks were higher at the V2-Rande site (inner zone), which may lead to better condition of cockles at Punta do Cabo, as reflected by higher CI values. At the same time, the late spawning period coincided perfectly with the peak concentration of Chl a recorded in autumn. The same results were found in the Ria de Arousa where C. gigas (Thunberg 1793) underwent a second cycle of sexual maturation associated with a phytoplanktonic bloom in late summer and early autumn (Ruiz at al. 1992). Also, on the coast of Malaga (southern Spain), several bivalve species spawned when there was a continuous increase in Chl a, although the seawater temperature was relatively low (Tirado & Salas 1999, Tirado et al. 2002, Tirado et al. 2003). Apart from supplying sufficient energy for gametogenesis, a major advantage of phytoplankton as a cue to spawning is that it integrates various environmental parameters, indicating favorable conditions for larval success (Ruiz et al. 1992). Moreover, this may be useful in the particular environmental conditions in the Ria de Vigo, where unusually high levels of Chl a occur in autumn, given its temperature and salinity regimes.

In conclusion, the spring spawning of the cockle C. edule in the Ria de Vigo occurs in response to a sharp increase in temperature, although in autumn it is the high concentration of Chl a that acts as a stimulus after the optimum temperature has been achieved. At the Punta do Cabo site, in the inner part of the ria, both lower salinity and greater maximum concentrations of Chl a provide favorable conditions that enable the cockle population to increase its reproductive effort, as reflected by greater CI values.

ACKNOWLEDGMENTS

This study was funded by the Xunta de Galicia (PGDIT01 MAR30102PR). We acknowledge a fellowship to C. M.-C. from the Ministry of Science and Technology. We thank INTECMAR for providing temperature, salinity, and chlorophyll a data, and thank AEMET for providing rainfall data. We are also very grateful to Jose Carlos Marino, Maria Espineira, and Esther Perez for their help with sampling and laboratory work; and to Fran Saborido-Rey and his group for their assistance in the histological tasks.

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C. MARTINEZ-CASTRO * AND E. VAZQUEZ

Dpto. Ecoloxia e Bioloxia Animal, Facultade de Ciencias do Mar, Universidade de Vigo, 36310 Vigo, Spain

* Corresponding author. E-mail: crismc@uvigo.es

DOI: 10.2983/035.031.0320
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