© 2006 International Council for the Exploration of the Sea
Morphometric and gonad maturity in the spider crab Maja brachydactyla: a comparison of methods for estimating size at maturity in species with determinate growth
Departamento de Bioloxía Animal, Bioloxía Vexetal e Ecoloxía, Universidade da Coruña Campus da Zapateira s/n, E-15071 A Coruña, Spain
*Correspondence to J. Freire: tel: +34 981 167000; fax: +34 981 167065. e-mail: jfreire{at}udc.es.
Ontogenetic changes in the relative growth of males and females of the spider crab Maja brachydactyla, a species with terminal moult and determinate growth, were analysed and related to their reproductive (maturity) status. Based on the allometry of cheliped size, two morphometric groups of males separated juvenile and adult phases. Juvenile males also showed two growth phases, immature (smaller ones, without spermatophores) and adolescent (with spermatophores). Size at gonad maturity in males (estimated as CL50) was 96.2 mm carapace length (CL). Histological analysis of males showed that >60% of morphometric juveniles and 100% of morphometric adults had spermatophores in the gonad. Females begin to develop gonads 2–3 months after the terminal moult. Size at morphometric maturity was estimated comparing two methodologies: the size at 50% maturity (CL50) and the median size of adult cohorts (CLM). In all cases the CLM size at maturity was greater than that resulting from the CL50 method, and, in contrast to the CL50 method, CLM was greater for females in all cases. Therefore, CLM reflects better the real size at maturity for M. brachydactyla. Owing to spatial segregation of adults and juveniles and the availability of morphological and morphometric methods to estimate maturity status, we suggest a combination of spatial closures and direct protection of juvenile habitat as management strategies alternative to minimum landing sizes.
Keywords: decapods, Maja brachydacta, maturation, morphometrics
Received 1 February 2005; accepted 3 March 2006.
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Introduction |
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 Top Introduction Material and methodsResultsDiscussionReferences |
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The spider crab Maja brachydactyla [Crustacea, Brachyura; the NE Atlantic species previously known as M. squinado; see Neumann (1998) for taxonomic status] is characterized by determinate growth consisting of two main post-larval phases: the juvenile or growth phase, and the adult or reproductive phase. These two phases are separated by a terminal moult, after which the individual reaches sexual maturity and stops growing (González-Gurriarán et al., 1995; Sampedro et al., 1999). At this moult, crabs undergo morphological changes as well as alterations in the relative size of the chelipeds in males and the abdomen in females (Teissier, 1933, 1935; Hartnoll, 1963; Sampedro et al., 1999), which make it possible to distinguish adults and juveniles. These changes in external morphology have been used by many authors to estimate maturity in this species (Le Foll, 1993; Le Foll et al., 1993; Sampedro et al., 1999) as well as in other majids (e.g. Somerton, 1980; Conan and Comeau, 1986; Comeau and Conan, 1992).
Estimated size at sexual maturity is key in the assessment and management of commercially exploited populations, and is often used as a benchmark to establish minimum catch and/or landing size. There are two problems involved in the determination of this parameter: (i) selection of a biological criterion to identify mature animals, and (ii) definition of a criterion and statistical methodology to estimate the size at the onset of maturity in a specific population.
In decapods, different criteria have been used to identify sexual maturity. Gonad maturity, based on the presence of spermatophores in males, and on the presence of sperm in the spermathecae or of a clutch in females, has been used to define sexual maturity (see Paul, 1992, for a summary and references). In many brachyuran species, gonad maturity does not necessarily coincide with functional maturity (defined as the capacity to mate effectively). Therefore, gonad maturity (defined as the physiological capacity to produce gametes) may not be sufficient to define functional maturity, which is a broader concept that should also include mating ability, which depends on physiological, behavioural, and morphological aspects. As the external morphological changes are those that mark the end of all the processes that determine maturity in majids and other decapods, this is the criterion that is commonly used to classify crabs as mature or immature (Somerton, 1980, 1981; Conan and Comeau, 1986; Paul and Paul, 1990; Paul, 1992; Sainte-Marie et al., 1995).
Estimates of the size at 50% maturity at the population level (CL50) are most frequently used to define reproductive state in decapods, based on classification of crabs in a sample into mature and immature and the estimation of body size in which 50% of the specimens are mature. This approach assumes that there is a sigmoidal relation between size and the percentage of mature crabs (Roa et al., 1999). The CL50 may be interpreted as the size at which a randomly chosen specimen has a 50% chance of being mature (Somerton, 1980). However, in animals with determinate growth that exhibit a halt in growth after maturity is reached, as is the case of M. brachydactyla, variability in the abundance of the different cohorts (or year classes) may result in inaccurate estimation of the CL50 obtained using point samples of juveniles and adults from different cohorts. Somerton (1981) described this problem and proposed an alternative method for animals that undergo the terminal moult, a method based on the median size of the adult year class.
The spider crab has been the object of partial studies regarding the criteria to be used in determining maturity, without considering gonad development in males. Only one study, however, deals with estimating the size at maturity of a population using the CL50 criterion (Sampedro et al., 1999). Nevertheless, because this species of majid has a terminal moult, this method may be an inaccurate measure of the reproductive state of the adult population. In this study, we attempt to provide accurate criteria for the determination of size at maturity in M. brachydactyla based on data obtained from sampling in the Ría de A Coruña over the course of two consecutive years. Our specific objectives were to: (i) determine the association between the process of gonad and morphometric maturity in male M. brachydactyla and the onset of the reproductive cycle; (ii) estimate the size at maturity of males and females of this population by the two methodologies described above, and to compare them in order to determine which is the best estimate, because it is critical for any management decisions; and (iii) analyse interannual variability (between year classes) in size at maturity.
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Material and methods |
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The study area was the Ría de A Coruña (8°22'W 43°21'N), a small oceanic bay located in the northwest of Galicia. Freire et al. (2002) and Corgos (2004) synthesized the structure and population dynamics of M. brachydactyla there. Monthly sampling was carried out from December 1997 to November 1999 using experimental traps with a 50-mm mesh. Sampling was in shallow water (5–20 m) in the inner and middle areas of the ría inhabited by juveniles and postpubertal adults, and in a deeper area (25–31 m) in the central channel, which is used as a migratory corridor by adults that have recently attained maturity and are heading towards deep habitats for mating (Freire et al., 2002; Corgos, 2004).
Each crab caught was examined and the following data recorded: sex; carapace length (CL measured with a calliper to the nearest 0.1 mm), measured between the point where the rostral spines join and the posterior end of the cephalothorax; the right cheliped height in males (RCH, in the posterior area of the dactyl insertion; left claw measurement was used in case of the absence of or regeneration of the right claw; Sampedro et al., 1999, showed no differences in size between claws; crabs without or with both regenerated claws were excluded from analysis); shape of the abdomen in females (juvenile females have a flat abdomen with undeveloped pleopods and adults have a domed abdomen; Sampedro et al., 1999), the macroscopic stage of the intermoult cycle (intermoult, premoult, early postmoult, according to the classification of Drach and Tchernigovtzeff, 1967, with some minor modifications; see Sampedro et al., 2003); and relative age (on the basis of the degree of epibiosis and carapace erosion; see Fernández et al., 1998) to differentiate the recent postpubertal adults from the crabs that had reached sexual maturity in previous years.
In order to analyse the reproductive stage of males and females between July 1998 and June 1999, a monthly sample was obtained to examine the gonads of adult females (n = 170) and of juvenile and adult males (n = 382 and 128, respectively) from the shallow and deep sampling areas. Juvenile females were not considered because gonad development starts after the terminal moult (Sampedro et al., 1999). Males of 60–160 mm CL were selected and divided into 20-mm size classes (with a final size class including crabs >160 mm). A maximum of ten males from each size class caught in the shallow area was taken to the laboratory each month. A maximum of five males from the three largest size classes was obtained in the channel (smaller crabs were not caught there). Females measuring >100 mm CL were selected and grouped into three 40-mm size classes. A maximum sample of five females from each size class caught in the shallow area as well as in the channel was taken back to the laboratory.
The specimens were dissected to determine gonad maturity stage. For females the classification proposed by González-Gurriarán et al. (1993, 1998), i.e. four stages of gonad maturity, was applied:
- Stage I. undeveloped gonads, white or light cream in colour;
- Stage II. developing gonads, cream to pale orange, oocytes with some yolk formation, mainly in the outer area;
- Stage III. gonads spreading widely through the cephalothoracic cavity, orange, and with large oocytes with abundant immature yolk and granulations of mature yolk that occupy most of the cytoplasm;
- Stage IV. completely mature gonads filling the cephalothoracic cavity, bright orange, with large, well-developed oocytes with clearly differentiated yolk granulations that occupy all the cytoplasm.
- Stage II. developing gonads, cream to pale orange, oocytes with some yolk formation, mainly in the outer area;
In the present study, only primiparous females that had recently attained sexual maturity and had not yet spawned were included. The presence of spermatophores was determined by examining a small crushed portion of the gonad under the microscope. The gonad from each crab was extracted and kept for 48 h at 60°C to obtain the dry weight.
Determination of morphometric maturity
The morphological change that occurs in the female abdomen during the terminal moult makes it possible to identify juveniles and adults (Sampedro et al., 1999). Because the onset of gonad maturity in females begins one or two months after the terminal moult, morphological maturity is a good indicator of sexual maturity (González-Gurriarán et al., 1993, 1998; Sampedro et al., 1999). In males, the relative growth of the chelipeds is used to discriminate between life-history stages (Sampedro et al., 1999). This study followed the statistical methodology used by Sampedro et al. (1999) with some minor modifications.
The allometry of the chelipeds (RCH) was estimated by simple linear regression using log10-transformed data:
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A principal component analysis (PCA) was carried out with the above variables (log10 RCH and log10 CL), allowing us to distinguish two groups of males that would represent juveniles and adults. Crabs were assigned to each group using a non-hierarchical classification procedure (K-means cluster). This method is based on establishing a predetermined number of groups (in this case, two) and assigning crabs to one of the groups according to their loads on the two axes of the PCA, by means of an iterative process that minimizes intra-group variance and maximizes between-group variance. Using the results of the classification, a discriminant analysis was conducted to obtain a discriminating function that permitted any crab to be classified as a juvenile or an adult on the basis of cheliped height and carapace length.
Males <80 mm were classified a priori as juveniles and excluded from the analysis (the probability of finding a <80 mm adult male is minimal) in order to generate better results for the discriminant analysis in the size range where juveniles and adults overlap.
Determination of growth phases in juvenile males
To determine whether there were different growth phases in juvenile males, as proposed for this and other majid species (Conan and Comeau, 1986; Sainte-Marie et al., 1995; Sampedro et al., 1999), we compared one- and two-stage relative growth models. Using piecewise linear regression with a breakpoint, two allometric equations were fitted and a breakpoint estimated. Fitting of the two-stage model was compared with a model based on only one phase using the F-statistic with 2 and n – P degrees of freedom:
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Estimating the size at morphometric and gonad maturity
Two criteria were used to determine morphometric size at maturity in males and females: (i) the size at 50% maturity (CL50) for which a logistic regression was performed relating body size (CL) and maturity stage (classifying specimens into juveniles or adults depending on their morphometry); (ii) the median size of adult cohorts (CLM) estimated using the complete sample for a given cohort. Both methods were applied independently to data from 1998 and 1999 and by pooling the two years. With regard to CL50, the data used included cohorts of adults that reached maturity in each year as well as different cohorts of juveniles that will reach maturity in the next two years.
The gonad maturity size, defined as the CL at which 50% of males carried spermatophores, was estimated by means of a logistic regression with a binomial likelihood function relating body size (CL) to the presence/lack of spermatophores.
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Results |
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In all, 14 983 crabs were caught: 7430 males (5888 juveniles and 1542 adults, classified using the discriminant function presented below), and 7553 females (5393 juveniles and 2160 adults, classified on the basis of abdominal morphology). Catch per unit effort (cpue) during the sampling period (Corgos, 2004) indicated peaks in juvenile recruitment in shallow water in autumn (October/November) and winter (January), and a lesser peak in summer (July). Postpubertal adult males were detected in shallow areas from April to October, and in the migratory corridor between September and November. Adult females were found in shallow water from July to December, and in the deeper zone between September and December. The indication from these results is that the juveniles caught between September and August and the adults caught from March to December belong to the same year class.
Male morphometric maturity and juvenile growth
The percentages of variance explained by the PCA performed using morphometric variables were 97.8% and 2.2% for axes I and II, respectively. According to the loads on axes I and II, each crab was classified into one of the two groups (adults or juveniles) using the K-means classification analysis. The discriminant function obtained to distinguish the maturity stage (Figure 1) was:
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In terms of juvenile male growth, a two-stage growth model had a better fit than a single relative growth model (F2,5873 = 889.81, p < 0.001). Using a piecewise linear regression, one equation was fitted to first-phase juveniles (the smaller ones, identified as immatures), and another to second-phase juveniles (identified as adolescents; Table 1, p < 0.001, r2 = 0.975; Figure 2). Adolescents had chelipeds with a higher allometric level than immatures, with slope values of 1.6 and 1.2, respectively. The CL at the breakpoint was 96.2 mm, so juveniles equal to or greater than that are considered adolescents and smaller ones as immatures.
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Male gonad maturity
Juvenile crabs used in gonad analysis ranged in size from 62 to 173 mm CL, and adults from 115 to 208 mm CL (Table 2). All morphometrically mature individuals had spermatophores, but they appeared in just 60.2% of juveniles. Juveniles with spermatophores present had a mean CL of 118.4 mm, whereas those without spermatophores measured 92.4 mm on average. Of juveniles, 71.5% of morphometrically immature animals did not exhibit spermatophores, whereas 76.7% of morphometrically adolescent specimens had them.
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Gonad maturity size, defined as the CL at which 50% of the males exhibited spermatophores, was estimated by means of the following logistic regression:
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Males attain gonad maturity at 96.2 mm CL, a size that coincides with the breakpoint separating immature individuals from adolescents. This indicates that males reach physiological or gonad maturity one or two moults before the terminal moult, after which they attain morphometric or functional maturity.
The gonad dry weight of adults was more than 10x greater than that of juveniles (mean gonad dry weights 1.1 g and 0.1 g, respectively). The gonad mass remained constant in juveniles over time, whereas in adults it increased rapidly between August and December (Figure 3). Adolescents had a mean gonad weight almost 8x higher than immature crabs (mean gonad dry weights 0.14 g and 0.02 g, respectively), although a seasonal pattern of gonad development was not detected (Figure 4). Consequently, although they did have spermatophores, there was no evidence of gonad development in juveniles.
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Female gonad maturity
In total, 163 morphometrically mature females were examined, 138 of which were caught in the inner area of the ría, and 25 in the central channel. They showed a clear seasonal pattern of gonad maturation. After the terminal moult, females had gonads in the early stages of development (between July and October, 93% of females are at stage I; Figure 5) and only in November did the females attain more advanced developmental stages (II and III). No females with gonads in an advanced stage of development (IV) were found in either the shallow area or the channel.
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In November and December, 58% of the females in the shallow area had gonads at stage II, and 19% at stage III. In the channel, 64% of the females had gonads at stage II, and 27% at stage III (Figure 5). Gonads began to mature between two and three months after the terminal moult, immediately before or during migration to deeper water. Gonad dry weight increased as the developmental stage advanced, so gonad development is reflected in a gradual increase in gonad weight over time (Figure 6).
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Size at morphometric maturity
Once the crabs had been classified into juveniles or adults using the morphometric methods described earlier, the size at morphometric maturity of the population was estimated. The sizes at maturity estimated through logistic regression (CL50) for the entire sampling period (Table 3) were 136.5 mm CL for males, and 130.3 mm for females.
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obtained for each year class and the whole sampling period for males and females. p < 0.001 in all cases. CL50 = –B0/B1. n is the sample size, and standard errors of the estimated parameters and the 95% confidence intervals for CL50 are also shown.When the median size of the adult cohort was used, the differences between the 1998 and 1999 year classes were 1.9 mm in males and 3.3 mm in females (Table 4). For the total sampling period, median CL was 139.9 mm and 148.7 mm in males and females, respectively. In all cases, the size at maturity obtained from the median of the cohort was greater than that resulting from the CL50 method, with differences of >20 mm. In contrast to the results of CL50, the median size at maturity of female cohorts was considerably greater than that of males (up to 11.2 mm in 1998), whereas the differences for each sex between year classes were minor.
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Discussion |
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Size at the onset of sexual maturity is one of the most important parameters of the life cycle of crustaceans to know, and its estimation has been attempted by many different methodologies. Traditionally, studies have been conducted on two processes related to maturity: reproductive capacity (gonad development, presence of spermatophores, etc.; Conan and Comeau, 1986; Paul, 1992; Sainte-Marie et al., 1995), and morphometric changes at maturity (Somerton, 1980, 1981; Conan and Comeau, 1986; Paul and Paul, 1990; Paul, 1992; Sainte-Marie et al., 1995). Methods based on reproductive capacity make it possible to determine the size at which a crab is physiologically mature. Morphometric changes, on the other hand, point to allometric changes in the growth of different parts of the body related to functional maturity, which enable the crab to mate.
In many brachyurans, male gonad maturity does not coincide with morphometric maturity (Conan and Comeau, 1986). In this study on Maja brachydactyla as well as in others on majids such as Chionoecetes opilio (Conan and Comeau, 1986; Sainte-Marie et al., 1995), C. bairdi and Paralithodes camtschatica (Paul, 1992), spermatophores were detected in the gonads of morphometrically immature specimens, which would imply that physiological maturity occurs prior to morphometric maturity in males. Physiological maturity in decapods usually takes place when the animals reach morphometric adolescence, one or two moults before morphometric maturity. Hartnoll (1965) stresses that the presence of spermatophores is only circumstantial evidence of maturity and that adequate demonstration of this would require mating experiments. Several laboratory studies have shown that morphometrically immature males of Chionoecetes and Paralithodes were capable of mating (Paul and Paul, 1990; Paul, 1992). Yet Conan and Comeau (1986) did not observe pre-copulatory behaviour in morphometrically immature animals as big as or bigger than morphometrically mature active specimens with spermatophores.
Male majids observed mating in the wild are usually morphometrically mature (Powell et al., 1972) and larger than females (Powell et al., 1972; Brosnan, 1981; Conan and Comeau, 1986; Ennis et al., 1988; Paul, 1992). Agonistic interactions have been observed prior to mating in the males of several decapod species (Stevens et al., 1993; Van Der Meeren, 1994; Elner and Beninger, 1995; Jivoff, 1997; Wada et al., 1997; Sainte-Marie et al., 1997, 1999; Rondeau and Sainte-Marie, 2001; Correa et al., 2003; direct observations by fishers on M. brachydactyla) during which large crabs may exclude smaller ones. Sometimes smaller males are rejected by females (Goshima et al., 2000), and it is possible that small males may not be able to mate with large females, because the allometric increase in the size of the chelipeds is also related to the role they play in supporting the female during courtship and mating (Brosnan, 1981; Rodhouse, 1984; Jivoff, 1997). Rodhouse (1984) performed laboratory experiments on M. brachydactyla in which he noticed that large males prevented smaller males from entering the baited traps. The same behaviour may prevail when crabs are competing for females.
These results for majid crabs would suggest that, although a morphometrically immature male might be physiologically mature, it is very unlikely that such an animal would be able to mate in the field. Moreover, of morphometrically mature crabs, the larger ones will have a competitive advantage over smaller ones and be able to mate with a greater number of females. Therefore, a male crab that has attained gonad maturity may not be functionally mature. In M. brachydactyla as in many other species, the production of spermatophores, and consequently gonad or physiological maturity, takes place prior to the terminal moult and/or morphometric maturity. Therefore, a morphometrically immature crab can potentially mate with a female (as demonstrated in laboratory studies; Sainte-Marie et al., 1997), but is unlikely to mate in the wild, and even more unlikely in the case at hand, because mating occurs during migration and in deeper water, to where juveniles do not migrate. In view of the above, it may be more appropriate to estimate size at maturity on the basis of morphometric criteria; as Hartnoll (1965) stated, experimental studies may bias the size at sexual maturity of wild populations.
In the Ría de A Coruña, M. brachydactyla females moult terminally in shallow water between June and September, with a peak in August (Corgos, 2004). However, we did not observe many crabs with gonads in advanced stages of development (II and III) until November. Therefore it is likely that gonads only begin to develop 2–3 months after the terminal moult. This pattern of gonad maturation is similar to that presented by González-Gurriarán et al. (1993) for the Ría de Arousa (150 km from the study area, in the south of Galicia), and by García-Flórez and Fernández-Rueda (2000) for the coast of Asturias (200 km north of the study area). In the present study no females were observed at development stage IV. In the Ría de Arousa, primiparous females were reported at stage IV from December onwards, and on the Asturian coast (where primiparous females were not differentiated from multiparous females), they were detected from October. The difference may be that, in the earlier studies, samples were taken from the commercial fishery which operates mainly in deep water, whereas in this study the females were caught in shallow water before they migrated.
In females of other majids such as C. opilio (Moriyasu et al., 1987; Elner and Beninger, 1992, 1995; Alunno-Bruscia and Sainte-Marie, 1998), C. bairdi (Donaldson et al., 1981), and Hyas coarctatus (Lanteigne et al., 1996), gonad maturation starts one or two moults before terminal moult, but the abdomen remains narrow and unable to carry a clutch. Moreover, full ovary development is only achieved after the terminal moult, so only mature females can reproduce. In such cases, size at maturity is also best described by morphometric maturity.
As M. brachydactyla stops growing once it reaches morphometric maturity, and it is possible to establish the relative age of adults, the median size of adult cohorts should be the best estimate of the size at maturity of the population (Somerton, 1981). This parameter has much less interannual variability than CL50 estimated using logistic regression with cross-sectional data, indicating that the median size of adults may be far more robust and less influenced by year-class strength of juveniles, as proposed by Somerton (1981).
The size at maturity obtained using the CL50 criteria for females in the entire sampling period is similar to that reported by Sampedro et al. (1999) for the Ría de Arousa (130.4 mm), and slightly higher in males (136.5 and 132.7 mm, respectively). On the other hand, García-Flórez and Fernández-Rueda (2000), who used the mean size of adult females as size at maturity, reported substantially smaller sizes (133.5 mm in 1997, 124.4 mm in 1998) on the Asturian coast than the results for the Ría de A Coruña (median sizes of 150.1 mm in 1998, 147.1 mm in 1999). These differences between proximate geographic areas may be caused by differences in sampling methods, because on the Asturian coast, samples from the commercial fishery were used and fishers generally discard recently moulted crabs with soft carapaces or less muscle mass. Both carapace hardness and muscle development require long periods in large specimens, so discarding tends to increase with body size, which may have biased the size at maturity obtained by García-Flórez and Fernández-Rueda (2000).
Currently, a minimum landing size of 120 mm CL is established in the Spanish fisheries for M. brachydactyla. Our results indicate that an important proportion of juveniles are larger than the minimum size. However, there is a large variability in size at maturity (the terminal size) within a cohort, and any realistic minimum size will cause a part of the adult cohort to be unfished. In the long term, the protection of small adults could generate a strong selective pressure on the size at maturity of exploited populations. Therefore, regulation based on cut-off sizes seems not to be an appropriate management strategy. Two aspects of the biology of M. brachydactyla could allow alternative strategies: spatial segregation of adults and juveniles, and the availability of morphological and morphometric methods to estimate the maturity status of any crab. In this sense, a combination of spatial closures and direct protection of juvenile habitat could be more effective at protecting juvenile cohorts without the undesirable selective side-effects of minimum sizes.
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Acknowledgements |
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We thank Juan Otero, Patrón of the vessel "Bolvina" for support, and Cristina Bernárdez, Paz Sampedro, and Patricia Verísimo for help with the fieldwork. Eduardo González-Gurriarán critically evaluated an early draft of the manuscript. The study was funded by research grants XUGA10301B97 funded by the Dirección Xeral de Universidades e Investigación, Consellería de Educación e Ordenación Universitaria, Xunta de Galicia, and REN2000-0446MAR funded by the Spanish Ministerio de Ciencia y Tecnología (MCYT).
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References |
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