Timing and seasonality of the terminal molt and mating migration in the spider crab, Maja brachydactyla: evidence of alternative mating strategies.

ABSTRACT Timing and synchronization at individual and population levels of the processes related to the terminal molt, gonad maturation, accumulation of energy reserves and migration in the spider crab Maja brachydactyla are analyzed. Also, the intra and intersexual variability is established. Two hypotheses are tested to explain the temporal and population variability: (1) physiological hypothesis: males and females begin migration when they reach the appropriate physiological stage (the optimum level of energy reserves) and (2) mating opportunities hypothesis: the timing of the migration maximize mating opportunities and mate quality. Our results show that males carry out the terminal molt before females, the former having a peak in July and the latter in August. The onset of gonad maturity in females occurs between two and three months after they have reached morphometric maturity (starting in October), coinciding with the period prior to and during the mating migration to deep waters. In an analysis of the spermathecae of primiparous females, it was found that practically no mating activity occurred in shallow waters, whereas the first copulations took place in the migration corridor. However, probably most of the mating activity occurs in deep mating grounds. Males reached gonad maturity prior to morphometric maturity. No differences were observed in the physiological status (muscle, gonad and hepatopancreas relative mass) between migrating and nonmigrating crabs, which is a clear indication that the physiological hypothesis does not hold true for this species. A higher percentage of postmolt crabs were caught in the migration corridor than in shallow waters. The physiological condition improved over time in males and females in the specimens caught in the shallow area as well as in the migration corridor. Therefore, the crabs that start migrating first did so in poorer physiological condition. Moreover, the early migrators had a significantly lower mean size than the late migrators. Our results suggest that variability within populations and between sexes are related to the different reproductive strategies and not to a physiological limitation. Thus, the poor-quality males (with a reduced competitive ability) would migrate at the beginning of the season to maximize the mating opportunities that would not be feasible if they had to compete with the late migrators, which are larger in size and in better physiological condition. Sperm competition is not clear in M. brachydactyla, but all evidences point at last male preference for fertilization of eggs.

KEY WORDS: decapod, Maja brachydactyla, mating, mating strategies, migration, reproductive migration

INTRODUCTION

Juveniles of Maja brachydactyla (Balss 1922, see Neumann 1998 for taxonomic status, corresponding to the North Atlantic species previously known as M. squinado) live primarily in shallow waters (Gonzalez Gurriaran & Freire 1994, Hines et al. 1995, Le Foll 1993, Meyer 1993, Sampedro 2001, Freire et al. 2002). During the summer of their second or third year of life (depending on the recruitment season) these crabs carry out the terminal molt, associated with the onset of sexual maturity [Corgos 2004, Corgos & Freire (in press), Corgos et al. (Submitted), Freire et al. 2002, Gonzalez-Gurriaran et al. 1995, Le Foil 1993, Meyer 1993, Sampedro et al. 1999]. Between late summer and early autumn adult specimens carry out a reproductive migration to deep waters as has been observed in different areas on the European coast (Camus 1983, Edwards 1980, Freire & Gonzalez-Gurriaran 1998, Freire et al. 1999, Gonzalez-Gurriaran & Freire 1994, Kergariou 1976, Kergariou 1984, Latrouite & Le Foll 1989, Le Foil 1993, Meyer 1993, Stevcic 1973). Although information is scarce on the mating behavior of the spider crab in the field, based on available evidence mating is known to take place mainly in deep waters, where aggregations could be formed (Gonzalez-Gurriaran et al. 2002). The terminal molt, gonad maturity, migration and mating are factors that are closely interrelated and play an important role in the life history of the spider crab, because they will determine drastic changes in the spatial structure and demography of the populations and are fundamental in terms of reproductive success.

It has been widely documented that migrating animals store energy reserves before they begin to migrate to ensure the success of the migration (Dingle 1996). In the spider crab, migration entails a drastic change in activity (rapid movements of over 1-10 km x [day.sup.-1], after a juvenile phase with only small-scale movements (10s or 100s m x [day.sup.-1], Bernardez et al. 2005, Freire & Gonzalez-Gurriaran, 1998; Gonzalez-Gurriaran & Freire, 1994; Gonzalez-Gurriaran et al. 2002; Hines et al. 1995). This migration, however, takes place after the terminal molt--a physiologically and energetically critical process. Therefore, during a short period directly after the molt and prior to migration, the processes related to the recovery after ecdysis and the storage of the energy needed for migration must be carried out. Differences between males and females in the timing of migrations in other geographic areas have been reported; particularly the fact that males start to migrate before females (Stevcic 1973). This differential behavior may be related to the reproductive strategies of the two sexes, as has been observed in other vertebrate species and other arthropods (Morbey & Ydenberg 2001).

Spider crab males compete for females, which gives rise to agonistic interactions (information based on direct observations by fishermen of occasional matings in shallow waters), and females may mate with several males (Gonzalez-Gurriaran et al. 1998). Information based on observations of the mating activity of crabs held in captivity and at sea would indicate that males and females mate in hard carapace condition (no mating has ever been observed immediately after the molt). It is possible for ovigerous females to mate, and courtship prior to copulation does not take place, nor does pre or postcopulatory mate guarding (Gonzalez-Gurriaran et al. 1998). This mating behavior differs from the characteristics defined for other majids (Claxton et al. 1994, Jones & Hartnoll 1997, Sainte-Marie et al. 1999). The fact that females have a hard carapace during mating determines the characteristics of the mating system. On the one hand, it means that the existence of mate guarding aimed at protecting females with a soft carapace from predators is not necessary for these crabs (e.g., Hartnoll 1969, Jivoff 1997a, Wilber 1989) and/or ensuring the paternity of the brood (Diesel 1991, Jivoff 1997a), although postcopulatory mate guarding has been observed in hard-shell females of Chionoecetes opilio (Claxton et al. 1994). On the other hand, in the case of the spider crab, all the adult females are receptive, which means that the operative sex-ratio, defined as the number of sexually active males versus the number of fertilizable females (Emlen & Oring 1977), is equal to the effective sex-ratio.

In other majids, sperm competition tactics that favors last male's paternity has been observed (Diesel 1990, Rondeau & Sainte-Marie 2001, Sainte-Marie et al. 2000), but this is not clear in M. brachydactyla, (Gonzalez-Gurriaran et al. 1998: Freire, unpublished data).

The timing and synchronization of the biological processes associated with reproductive migrations, at the individual and population levels, and the sexual differences observed in the spider crab may be explained by 2 sets of alternative hypotheses:

   Physiological hypothesis: males and females start migrating
   when they have reached the appropriate physiological status
   (an optimum level of energy reserves). Therefore the variability
   within populations and sexes would be related to the
   physiological stage, depending on the timing of the terminal
   molt and the energy recovery rate. Both processes may be
   variable between sexes, with the energy needed lot reproduction,
   and among body sizes.

The physiological hypothesis could be tested using the following predictions: (1) The physiological condition of the postpubertal adults caught in the migration corridor would be better than that of crabs still remaining in shallow waters. This pattern should be observed throughout the entire migration period. The physiological condition during the migration season would improve gradually in crabs from shallow waters, whereas it would remain relatively constant in time in individuals captured in the migration corridor (Fig. 1). (2) Sexual differences in timing would depend on the differential physiological condition of each sex, related to differences in the timing of the terminal molt.

[FIGURE 1 OMITTED]

   Mating opportunity hypothesis: the timing of the migration
   should maximize mating opportunities and mate quality.
   Once a minimum physiological condition is reached, males
   would migrate at the appropriate time to intercept and mate
   with the greatest possible number of females in the mating
   habitats (in the spider crab these would include zones where
   females may be intercepted during migration and/or in deep
   waters). The variability within populations and sexes would
   be related to different reproductive strategies and not to a
   physiological restriction (possibly once a minimum level of
   energy reserves has been reached). According to this hypothesis,
   the intrasexual variability would be determined by
   the interindividual differences in quality.

The mating opportunity hypothesis could be tested using the following predictions: (1) At any given moment, crabs in migration and in shallow waters would not necessarily exhibit any differences in their physiological condition. (2) Poorer quality males (in the case of crustaceans, animals having a smaller body size and/or lower robust physiological condition) would carry out migration earlier to maximize the possibility of mating encounters before high-quality males arrive to the mating grounds. Therefore, the physiological condition would improve throughout the migration period in both shallow waters and the migration corridor.

From the standpoint of males, mating probability depends on the abundance of females and on the competition among males, which means that the temporal distribution of mating opportunities throughout the season is probably unimodal. At the beginning, mating probability would be low owing to the absence of females in the mating zones. As females start arriving, these odds would likely increase until they reach a maximum value, then the probability would diminish, because the density of males would attain a maximum and the competition among them would cause mating probability to decrease (Fig. 2).

[FIGURE 2 OMITTED]

According to the mating opportunity hypothesis, early migrating males would be smaller and have a poorer physiological condition, but they would be the first to arrive at the mating zones. Besides being able to mate with females during migration, they would have a higher probability of mating with the first females to arrive at the mating zones (Fig. 2, A). The density of females would increase over time, but so would the density of males, so the percentage of intercepted females would gradually decline because of the competition (Fig. 2, B), until it reaches a minimum level that would coincide with the maximum density of males (Fig. 2, C).

Late migrating males would arrive at the mating zones later, but they would be larger in size and in stronger physiological condition (high quality males), which means that they would be better competitors than the early migrators. As density of females increases, the mating probabilities of these males would increase (Fig. 2, B) until a maximum value is reached, coinciding with the maximum density of females in the zone (Fig. 2, C).

For females the optimum strategy would be to mate with the males of the best quality available at any given moment. Males with larger ornaments or weapons, greater body size, or higher rates of courtship showed greater survivorship or longevity (Jennions et al. 2001). From this standpoint late migrants should be genetically superior, conveying genetic benefits to females by rising the mean offspring fitness caused by inheritance of "good genes," that may enhance survivorship or longevity of offspring and increase the sexual attractiveness (Jennions & Petrie 2000).

This study is a detailed analysis of the timing and synchronization at the individual and population levels of processes related to the terminal molt, gonad maturation, accumulation of energy reserves and migration in the spider crab. Intra and intersexual and intrapopulation variability in the earlier mentioned processes are analyzed. Our results will allow comparison, at least in part, the hypotheses proposed earlier related to the causes of the timing and synchronization of the processes linked to migrations.

MATERIAL AND METHODS

Monthly samplings were carried out between December 1997 and November 1999. From late summer until autumn, sampling effort was increased to obtain more detailed information on the migration of adults. Sampling was carried out using experimental traps (50-cm height, with upper and lower diameters of 110 cm and 100 cm respectively, and an entry of 22 cm and a 50-mm mesh, Corgos and Freire, submitted a). Soak time was 24 h and traps were baited with fresh horse mackerel (Scomber scombrus). The sampling area was the Ria de A Coruna, a small oceanic bay located off the NW coast of Galicia (NW Spain). One shallow water (5-15 m) sampling station was selected in the inner area of the ria (Bastiagueiro) and another one in deeper waters (25-30 m) in the central channel of the ria, which constitutes the migration corridor for postpubertal adults. In the inner area of the ria, where there is high abundance of Maja brachydactyla, sampling was carried out along a transect on the longitudinal axis of the ria where seven tows were carried out deploying the traps parallel to the coast. Tows were separated approximately 180 m from each other (Fig. 3).

[FIGURE 3 OMITTED]

The following data were recorded for each specimen captured: sex, morphometric maturity (Corgos 2004, Corgos & Freire, in press, Sampedro et al. 1999), stage of the intermolt cycle (estimated by the hardness of the exoskeleton and the presence of a new internal carapace in crabs approaching molt, Sampedro 2001) and the relative age based on the degree of epibiosis and carapace wear (see Fernandez et al. 1998), to distinguish the recent postpubertal adults from specimens that had reached maturity in previous years.

To analyze the reproductive stage and physiological condition of males and females, adult females and juvenile and adult males were sampled monthly from July to December 1998 (morphology of the abdomen allow to determine the maturity stage directly in females; Sampedro et al. 1999). The maturity stage of males was determined later based on their morphometry. Samples were obtained from shallow areas and the central channel, although for several reasons in the channel data were obtained only for females in September and November, and for males in November. Males with CL > 60 mm were selected and divided into size classes of 20 mm with a final class of specimens of over 160 mm. A sample made up of a maximum of 10 males belonging to each size class captured in the shallow area was transported to the laboratory. A sample of five males from the three larger size classes was obtained from the captures in the channel, because smaller-sized crabs were not caught in this area. Adult females with a CL > 100 mm were selected and grouped into size classes of 40 mm and a sample of 5 specimens from each size class of crabs caught in the shallow area and the channel was taken to the laboratory.

The crabs were dissected to determine the gonad maturity stage in females (following the classification proposed by Gonzalez-Gurriaran et al. 1993, Gonzalez-Gurriaran et al. 1998), gonad dry weight, fullness and the number of sperm masses in the spermathecae in the case of females (following the classification proposed by Gonzalez-Gurriaran et al. 1993, Gonzalez-Gurriaran et al. 1998), and the presence of spermatophores and gonad dry weight in males. The gonad, hepatopancreas and the muscle of the second right-hand pereiopod of each specimen were extracted and held for 48 h at 60[degrees]C to obtain the dry weight (Corgos & Freire, in press). Morphometrically juvenile males were omitted from the analysis of the physiological condition.

Data Analysis

The energetic status of each individual was estimated by means of condition indices (CI) based on the dry weight of the gonad, muscle and hepatopancreas. The condition indices were estimated as the residuals of an allometric regression (Log Y = log a + b x log CL) of the dry weight of each type of tissue respect to the carapace length (Fig. 4). The regressions were fitted to the data from the adult specimens caught between June and December 1998. Multiparous adults and juveniles were not included in the analyses.

[FIGURE 4 OMITTED]

The differences in the condition indices between migrators and nonmigrators over time, according to the predictions from the hypotheses, were analyzed using the time series corresponding to the condition indices of the crabs captured in shallow waters was fit to a second order polynomial regression: CI = a + b x date + c.[date.sup.2]. Next, the condition index from specimens captured in the channel (these data were only obtained in some of the months) were compared with the trend of data from Bastiagueiro. Significant differences between the two areas were accepted when the mean CI of the channel fell outside the 95% confidence band of the regression for the shallow area.

The molt stage was used as an additional body condition indicator, because the crabs in postmolt are in poorer condition than those in the intermolt or premolt stage. The differences in the molt stage between migrators (early and late) and nonmigrators were determined by means of a log-linear analysis on the frequency of males and females in postmolt in Bastiagueiro and in the channel in September and October 1998.

An analysis of variance (ANOVA) was performed to test differences on the mean body sizes of the migrators and nonmigrators, using data from males and females caught in Bastiagueiro and the channel in September and October 1998.

RESULTS

Seasonality and Sexual Differences in the Terminal Molt

Adult males in postmolt began to appear in the catches from Bastiagueiro in April, with their abundance undergoing a rapid increase, reaching high levels in June and a maximum in July. In September, the abundance of postmolt adults dropped sharply and continued to decrease more gradually until the complete disappearance of these crabs in December (Fig. 5). Postmolt females started to be caught in shallow waters in July, attaining maximum abundance in August. They dropped sharply in September and had practically disappeared by October (Fig. 5). The pattern was repeated in 1998 and 1999 and males were found to carry out the terminal molt one month earlier than females. The maximum numbers of postmolt adult males and females were found in July and August respectively. The terminal molt period in males lasted longer than in females (postmolt males were found from April until November in 1998). In 1999, there would seem to be greater synchronization, because adult males started to be caught in June.

[FIGURE 5 OMITTED]

Gonad Development and Mating

Adult females showed a clear seasonal pattern of gonad maturation. After the terminal molt, females had gonads in the early stages of development (between July and October 93% of the females were in stage I) and until November females did not attain more advanced developmental stages (II and III). No females were found with gonads in an advanced stage of development (IV) in either the shallow area or in the channel. In the channel 64% of the females had gonads in stage II and 27% in stage III between November and December. Therefore in females the gonads began to mature between two and three months after the terminal molt, during the period immediately proceeding or during their migration to deep waters.

The analysis of the spermathecae of primiparous females revealed that the number of matings in the shallow zone was low, because 97% of females (n = 124) showed empty spermathecae. An increase in mating frequency was observed in the channel, given that over 21% of the females studied (n = 23) had mated. These results would indicate that mating may be carried out in the migration corridors, but most likely it is in the deep waters where most of the mating activity takes place (Table 1). All the females analyzed exhibited a single sperm mass. In the shallow area, in contrast, two multiparous females that were captured had 7 sperm masses in each spermatheca, presenting differences in color and volume, which would point to the existence of long intervals between matings (Gonzalez-Gurriaran et al. 1998).

After examining the gonads of the male crabs, it was evident that, unlike the females, gonad maturation takes place prior to morphometric maturity. Over 60% of the juveniles examined (n = 382) had spermatophores, and more than 76% of the juveniles with a CL > 96 mm as well as all of the morphometrically mature crabs had spermatophores. Therefore, males are functionally mature and ready to mate immediately after the terminal molt (see Corgos & Freire, submitted a).

Sexual Differences in the Timing of the Start of Migration

Based on the sampling carried out in the inner ria, it was possible to carefully monitor the small-scale movements of the adults and the start of their migration (Fig. 6). In July 1998 the mean CPUE of males was much greater than that of females (4.2 and 0.5 crabs x [trap.sup-1] respectively). Males were also found to be sparse around the innermost part of the ria and near the shoreline. In August the average CPUE of females found in the inner ria increased (3.8 crabs x [trap.sup.-1]), and males had moved to the outermost zone near the channel. By September, the large concentration of males in the outer part of the inner area had disappeared, which would imply that they had started migration, whereas the females had moved to the outer zone. In October, the few males left in the area started moving to the outer zone and leaving the area, whereas the females were concentrated in the outer part of the shallow area. In November, the catches yielded few adults, although some females were still found in the outermost area, which means that the females migrated between October and November. By December practically all the adults had left the area.

[FIGURE 6 OMITTED]

The catches taken in the channel confirm this seasonal migratory pattern (Fig. 7). They were concentrated in the months of September and October; however maximum catches of males were obtained in September and those of females in October. Males exhibited stable catches between September 25 and October 23 (Fig. 7). The first females, on the other hand, were caught on September 25, from which time catches increased gradually until they reached a clear peak on October 23.

[FIGURE 7 OMITTED]

Body Condition at the Start of Migration

From July to December, adult males in Bastiagueiro underwent a progressive increase in the relative weight of the muscle, gonad and hepatopancreas (Fig. 8). It was only possible to compare the physiological condition in the channel zone (migrators) and shallow area (nonmigrators) in November. During this month migrators presented condition indices similar to those of nonmigrators in all the tissues analyzed.

[FIGURE 8 OMITTED]

The condition index in females found in the shallow areas showed a gradual increase in the case of the gonad, but this was not so in the case of the muscle or hepatopancreas (except for very low values in the latter tissue in September). The adult females captured in the channel had slightly higher gonad condition values in November as compared with the shallow zone, whereas no differences were observed in September (Fig. 9). The physiological condition of the muscle was similar in November, which was the only month in which information was available for the channel. The physiological condition of the hepatopancreas, however, was similar in the two areas in September and November.

[FIGURE 9 OMITTED]

The percentage of postmolt males and females in each zone was higher in September than October (Table 2), and in both months the percentage was higher in the channel than in Bastiagueiro (log-linear analysis of the effects of sampling station, date and sex on the percentage of specimens in the postmolt stage, showed the significant variables to be sampling station and date, [X.sup.2] = 5.53, P = 0.35). This would imply that the condition of the early migrators is poorer than crabs that migrate later.

Body Size at the Start of Migration

The mean size (CL) of males and females was compared between Bastiagueiro and the channel in September and October. Females were significantly larger than males, and in Bastiagueiro as well as in the channel for males and females, the largest sizes were found in October (ANOVA, n = 1198; effect of date and sex, P < 0.001; effects of sampling station and all interactions, P > 0.2). None of the interactions proved to be significant, which was an indication that the smaller-sized specimens of males and females started migrating earlier (Table 3).

DISCUSSION

This study provides evidence as to the existence of synchronization in the timing of the terminal molt, gonad development and migration in the spider crab. The inter- and intra-sexual differences related to these phenomena may reflect different types of behavior and reproductive strategies that would be compatible with the mating opportunity hypothesis discussed earlier. However, our results contradict some of the predictions made in the physiological hypothesis. To mate, an organism must be in the appropriate physiological condition, as well as having a suitable location in space and time (Correa & Thiel 2003). In M. brachydactyla, males probably reach maturity and develop gonads before females to be physiologically prepared to mate at the time and place where the encounter with the adult female occurs. Considering the date when migration starts and the fact that in December and January, ovigerous females begin to appear in the catches in the shallow areas (unpublished data), aggregation and mating in deep waters must occur over the course of a short period. Because females have spermathecae, they are able to mate when their gonads are in early stages of development, fertilizing the broods later.

In the Ria de A Coruna, the terminal molt takes place in shallow waters between April and August. Males undergo the terminal molt one month earlier than females. Gonzalez-Gurriaran et al. (1995) obtained similar results with this species under culture conditions, whereas in more northern latitudes, the cycle is delayed, owing possibly to the differences in the thermal regimen. In the English Channel the crabs undergo the terminal molt in late summer and early fall and adults that have recently reached the post-pubertal stage start to be captured in August-September, presenting maximum catches in early fall (Le Foll 1993, Meyer 1993).

An analysis of the captures in the channel during the migration shows that over the entire period males and females migrated, as would be expected in a species where the females are polyandric (Zonneveld 1992). In view of the captures obtained in the migration corridor, males showed stable catches during the migration period without a specific peak, whereas females, which started migration at the same time as males, exhibited a clear peak on October 23, 1998, after which catches were virtually nonexistent. These results indicate that the migration of males is not as synchronized as that of females, rather males carried out migration gradually over a 30-day period, whereas most females migrated between October 15 and 28, 1998.

Mating takes place generally after migration, in the deep-water wintering habitats, although copulation could occur also during migration (21% of the females caught in the channel had sperm in the spermathecae). These data largely coincide with those reported by Gonzalez-Gurriaran et al. (1998) in the Ria de Arousa, where the spermathecae of 100% of the primiparous females caught in the shallow zone were found to be empty. On the other hand, catches of multiparous females having several sperm masses, along with direct observations by fishermen, support the hypothesis that mating does occur in shallow waters, but probably restricted to multiparous females. In latitudes located farther to the north, matings were observed in shallow waters from May to July on the Irish coast (Brosnan 1981), and starting in June on the French coast (Kergariou 1984). Based on these observations, these authors report that mating generally occurs in summer, although to support this hypothesis, it would be necessary to carry out an analysis of the spermathecae content of females in wintering habitats.

The analysis of catches in the shallow area and the migration corridor and condition indices may be used as indicators of the reproductive strategies of M. brachydactyla. The condition indices of the tissues analyzed were similar in the shallow area and the migration corridor (i.e., no differences were observed in the body condition between migrators and nonmigrators), which would clearly imply that the physiological hypothesis is not supported in this case. The physiological condition increased over time in males and females both in crabs caught in Bastiagueiro and the migration corridor. Consequently, crabs that migrate first, do so in poorer physiological condition. Moreover, the early migrators were smaller in size than the late migrators. These evidences support the mating opportunity hypothesis. Poorer quality males (smaller sized and in poorer physiological condition) migrated earlier, which gives them mating opportunities that would not be feasible if they had to compete with the late migrators that are larger in size and in better physiological condition.

In both majids (Conan & Comeau 1986, Elner & Beninger 1995, Ennis et al. 1990, Sainte-Marie et al. 1997, Rondeau & Sainte-Marie 2001, Stevens et al. 1993) as well as other decapods (Correa et al. 2003, Jivoff 1997b, Van Der Meeren 1994, Wada et al. 1997) agonistic interactions have been observed between males prior to mating, in which the large-sized individuals exclude the smaller ones. At other times the small males are rejected by the females (Goshima et al. 2000). For this reason the larger-sized males are more likely to mate than the smaller-sized animals. This hypothesis is corroborated by observations in the field, where mating majid males were seen to be generally larger than the females (Brosnan 1981, Conan & Comeau 1986, Ennis et al. 1988, Paul 1992, Powell et al. 1972).

The less competitive (smaller-sized) male decapod crustaceans tend to avoid direct agonistic encounters with larger males (Clark 1997, Ra'anan & Sagi 1985) and they adopt alternative mating strategies, such as intercepting females moving to the mating areas (Van Der Meeren, 1994) or copulating quickly, whereas two dominant males are competing for a receptive female (Clark 1997, Correa et al. 2003). In this study the less competitive males migrated earlier to the mating zones, probably to be able to copulate before the more competitive males arrived.

In other majids such as Chionoecetes opilio (Sainte-Marie et al. 2000) and Inachus phalangium (Diesel 1990), the sperm masses are stored dorsoventrally in the spermathecae when they are not too full (i.e., the last sperm mass is stored closer to the oviduct). This stratification favors that the sperm of the last male fertilize the brood, and therefore the paternity is attributed to only one male. In both species males used several strategies to promote their own paternity. Males of C. opilio invest more sperm in females that had mated previously than in virgin females to displace and isolate the sperm deposited earlier (Rondeau & Sainte-Marie 2001), whereas males of 1. phalangium displace previously deposited masses by transferring large amounts of seminal plasma, which hardens forming a gel that completely seals off the previously deposited masses (Diesel 1990). All of these strategies favor the paternity of the last male to mate with a female. In our study, the high-quality males (larger and in better physiological condition) would be the last to mate. In M. brachydactyla, however, the arrangement of the sperm masses is different than what was observed in the previously mentioned species. When several masses are present, they are arranged parallel to the main axis of the spermathecae, and if the spermathecae are full, the arrangement is not stratified (Gonzalez-Gurriaran et al. 1998; Freire, unpublished data). Although all of these authors reported some differences in the size of the masses, they were attributed to different storage time or the possibility of having been used in part to fertilize a brood, and not to the existence of sperm competition. Based on these findings, there is no evidence that the last males to mate (those of better quality) have a greater probability of ensuring their paternity. However, the results of this study seem to suggest that high-quality males will inseminate females after these might have received sperm from low-quality males. This would only be a successful strategy if last males have fertilization advantages in M. brachydactyla. Future studies are required to examine whether sperm precedence in this species follows the same pattern as suggested for other majid species (i.e., last male precedence). The present results of diverging tactics of males during mating migration also seem to call for this pattern in M. brachydactyla.

ACKNOWLEDGMENTS

The author thanks Juan Otero, Skipper of the vessel "Bolvina;" Cristina Bernardez, Paz Sampedro, for their help in fieldwork and Martin Thiel, whose suggestions considerably improved the manuscript. This study was funded by research grants XUGA10301B97 from the Direccion Xeral de Universidades e Investigacion, Conselleria de Educacion e Ordenacion Universitaria, Xunta de Galicia, and REN2000-0446MAR funded by the Spanish Ministerio de Ciencia y Tecnologia.

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ANTONIO CORGOS, PATRICIA VERISIMO AND JUAN FREIRE *

Departamento de Bioloxia Animal, Bioloxia Vexetal e Ecoloxia, Universidade da Coruna, Campus da Zapateira s/n E-15071 A Coruna. Spain

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

TABLE 1.
Temporal evolution of spermathecae repletion (percentage of
specimens with sperm) of primiparous females in shallow water
and the in migration corridor of the Ria de A Coruna.

         Shallow Water   Migration Corridor

           N       %         N       %

Jul 98     20    10.0
Aug        19     0.0
Sep        32     0.0        9      0.0
Oct        24     0.0        1      0.0
Nov        15     0.0       11     45.5
Dec        14     7.1        2      0.0
Total     124     2.4       23     21.7

TABLE 2.
Monthly percentage of adult males and females in postmoult (stage
B) captured in Bastiagueiro and in the migration corridor in the
migration period. Sample size is indicated in each case.

                                                    % in
Date           Sampling Station     Sex       N     Postmoult

September 98   Bastiagueiro         Males     129      8.5
                                    Females   252      2.4
               Migration corridor   Males      87     11.5
                                    Females    73      9.6
October 1998   Bastiagueiro         Males      94      1.1
                                    Females   250      0.4
               Migration corridor   Males      97      4.1
                                    Females   201      4.0

TABLE 3.
Mean size (Carapace length, CL, with standard deviation, SD) of
the adult males and females captured in Bastiagueiro and in the
migration corridor at the start of migration. Sample size is
indicated in each case.

                                                         CL

Date           Sampling Station       Sex      N     Mean    SD

September 98   Bastiagueiro         Males     134   138.9   14.63
                                    Females   258   148.7   11.25
               Migration corridor   Males      87   139.9   11.19
                                    Females    72   150.8   11.34
October 1998   Bastiagueiro         Males      95   144.0   14.13
                                    Females   254   151.4   12.91
               Migration corridor   Males      97   143.0   13.38
                                    Females   201   152.2   12.30