Eduardo González-Gurriarán

Morphometry and Sexual Maturity in the Spider Crab Maja Squinado (Decapoda: Majidae) in Galicia, Spain

Ontogenetic changes in the relative growth of males and females of the spider crab Maja squinado were analyzed and related to their reproductive (maturity) status in order to define criteria to assign individuals to each growth phase. The sampling was carried out in two different areas of southern Galician waters, northwestern Spain, in shallow water ( 20 m) with soft bottoms (adult habitat). A Principal Component Analysis (PCA) of morphometric variables and a nonhierarchic K-means cluster of PCA scores differentiated two morphometric groups defined as juvenile and adult phases. A significant change in allometry of cheliped size was detected in juvenile males with a break point at a 109-mm carapace length (CL). This point may indicate a change in the relative growth of juveniles, separating the immature and adolescent phases. Histological analysis of a subsample of males showed that sperm were present in most adolescent crabs, but not in immature crabs. Bivariate morphometric linear discriminant functions allow for the identification of juvenile and adult males (classified previously by K-means cluster) with over 99% correct classification using CL and the length or height of the right cheliped. Carapace length at the onset of sexual maturity was estimated to be 132.7 mm (50% of adult males), although in a broad range, 112-165 mm, the size of juveniles and adults overlap. The life history of male spider crabs shows 3 phases differentiated by the relative growth rate of chelipeds separated by two 2 critical molts: prepubertal molt (immature-adolescent) determines a slight increase in allometry, and pubertal or terminal molt (adolescent-adult) determines an increase in the relative size and allometry of chelipeds and the onset of functional maturity. Females showed only 2 phases separated by the terminal molt. Growth of chelipeds in females showed no changes in allometry and was similar to juvenile males. Juvenile females presented a smaller relative width and a higher allometry of the abdomen with regard to adult females. Unlike juvenile females with a flat abdomen, adult females with a domed abdomen have well-developed pleopods, gonads, and seminal receptacles. Carapace length at the onset of sexual maturity was estimated to be 130.4 mm (50% of adult females). The range of overlap of the size of juveniles and adults (114-143 mm) was smaller than in males. The spider crab Maja squinado (Herbst) inhabits the Northeast Atlantic from the British Isles to Guinea and the Mediterranean Sea (de Kergariou, 1984; Le Foll, 1993). It is subject to an intense fishery, especially in the waters along the coast of the English Channel and Galicia, northwestern Spain. As for other species of the Majidae, the postlarval life history of Maja squinado consists of two main phases, growth and reproduction, which are separated by a terminal molt (Vernet-Cornubert, 1958; Hartnoll, 1963, 1978; Conan and Comeau, 1986; Comeau and Conan, 1992; Meyer, 1993; Gonzalez-Gurriaran et al., 1995; Freire et al., in press). The first morphometric study done on this species (Teissier, 1935) distinguished three main developmental phases in males, separated by two critical molts. In males, the most obvious morphological change throughout growth is the development of the chelipeds. This led morphometric studies to be based primarily on changes in relative growth rates, or allometric levels, of different variables measuring the size of the chelipeds. Females undergo changes in morphology and in the allometry of the width of the abdomen. Later, these changes in external morphology were used in growth and maturity studies of other species of the Majidae (Vernet-Cornubert, 1958; Hartnoll, 1978; Conan and Comeau, 1986). In studies carried out on other majids, the different phases of the life history and critical molts were based on morphological, morphometric, physiological (gonad maturation), and behavioral criteria (Fig. 1). In males, the first postlarval phase, known as immature or juvenile, gives rise to a second phase, known as prepubertal, juvenile, or adolescent, after a prepubertal, pubertal, or juvenile molt.

Mating and role of seminal receptacles in the reproductive biology of the spider crab Maja squinado (Decapoda, Majidae)

The reproductive biology of the spider crab Maja squinado was analyzed based on monthly samples from an 18-month study carried out in Galicia (NW Spain) and laboratory experiments holding primiparous and multiparous females in captivity with and without males. The seminal receptacles of adult females were analyzed and their relationship with the presence and developmental stage of the eggs and the gonad maturity stage was determined. Gonad maturation in primiparous females began one or two months after the pubertal moult. Females having gonads in an advanced stage of development made their appearance in December and the first spawning took place in mid-winter or early spring. The percentage of ovigerous females from March to September was ∼75%. As the incubation period progressed, the ovaries became mature again in order to carry out the next spawning. Under experimental conditions the breeding cycle started earlier in multiparous females, during their second yearly cycle, than in primiparous ones. After mating, female spider crabs store sperm in seminal receptacles and this sperm is used in the fertilization of eggs immediately prior to spawning. The analyses of seminal receptacles consisted of the estimation of fullness and the number of differentiated sperm masses. The number of masses ranged between 0 and 6 in field samples (median for females with stored sperm=1) and was positively correlated with fullness. Differences in colour and volume of individual masses showed that, at least in some cases, females carried out successive matings with long intervals in between. This storage mechanism allowed females to fertilize successive broods without remating (as was also shown under experimental conditions). Juvenile females from shallow waters did not have developed seminal receptacles which indicated that mating was not possible until the onset of maturity. Postpubertal females in shallow waters (August to October), including animals participating in aggregations, always showed empty receptacles. The seasonality of receptacle fullness showed that mating involved hard-shelled females and occurred in deep water during the autumn migration from juvenile habitats or in the wintering habitats, during the last stages of gonad maturation (November to February). After fertilization ovigerous females continued to store sperm, but the volume was lower than in non-ovigerous females. Mating may occur in ovigerous females, particularly in the final period of incubation, because in females with broods almost ready to hatch, both new and older sperm masses were seen in the receptacles (distinguished by colour and size). The fullness of the receptacles decreased both in ovigerous and non-ovigerous females in the final phase of the annual breeding cycle (August–October), however, some sperm was still available. In the laboratory, mating was observed, and no courtship nor postcopulatory guarding was recorded. The analysis of receptacles from laboratory experiments indicated that primiparous and multiparous females showed differences in the seasonality of mating in the first phase of the breeding cycle (September–January), related to differences in the timing of gonad maturation and hatching. Mating occurred in the final stages of gonad maturation, a short time before hatching, and matings were detected in ovigerous females. Multiple matings were also evident, to a greater extent than in the field, probably due to the higher availability of males. Females underwent over four successive spawnings in the laboratory without having to recopulate, and the incubation lasted on the average from 40 to 58 days (∼18 and 16°C respectively) and the mean duration between hatching and the next spawning was 3.4 days. It is estimated that most females carry out three successive spawnings during the annual cycle.

Growth at moult and moulting seasonality of the spider crab, Maja squinado (Herbst) (Decapoda: Majidae) in experimental conditions: implications for juvenile life history

Abstract Prepubertal growth (moult size increment and duration of the intermoult period) and the seasonality of moulting in the spider crab Maja squinado from the southern coast of Galicia (NW Spain) were analyzed under experimental conditions (laboratory and extensive culture). Two annual moult periods were observed; the first corresponded to the prepubertal moults that take place in spring (reaching their peak at the end of March and in April), and the second to the pubertal (terminal) moult in summer during which time the animals reach morphometric maturity. The peak for the terminal moults within the population took place in June in the experiment under extensive culture conditions and in July and August in the laboratory and in the field, where the maximum annual temperatures were lower and occurred later (17–19 °C in August and September) than in the former experiment (21–22 °C in July). The modal number of annual moults per crab was 2, and ranged between 1 and 3. The number of annual moults decreased with the size of the animal at the beginning of the moulting season, and the animals delayed ecdysis in accordance with body size (there was a significant positive correlation between moulting date and body size within each of the two periods). There were no significant differences between males and females in moulting seasonality. In the laboratory, the duration of the intermoult period prior to the pubertal moult was estimated to be 104 days, and for the prepubertal moult it was 85 days. For specimens between 60 and 130 mm carapace length (CL), the moult size increment was estimated to be an average of 29 mm CL, which constitutes an average of 32% of the pre-ecdysial size. There were no significant differences in the moult increment between sexes or between the laboratory and extensive culture experiments. There were however significant differences between the pubertal and non-puberty moults (27 and 36%, respectively). This was due to the larger sizes of the prepubertal animals, and to the negative correlation between body size and the percentage moult increment (the absolute moult size increment was positively correlated with CL). The samplings carried out in juvenile habitats in shallow areas in the outer part of the Ria de Arousa (Galicia, NW Spain) in summer and winter confirm these experimental results. The body size and intermoult and maturity stages of the animals caught indicate that most of the juveniles (mean CL ≈ 110 mm) carried out the terminal moult in summer and had moult increments similar to those in the experimental conditions (mean body size of postmoult mature animals was aproximately 140 mm). In winter, however, the population was mainly composed of juveniles in intermoult.

Management strategies for sustainable invertebrate fisheries in coastal ecosystems of Galicia (NW Spain)

Artisanal coastal invertebrate fisheries in Galicia are socio-economically important and ecologically relevant. Their management, however, has been based on models of fish population dynamics appropriate for highly mobile demersal or pelagic resources and for industrial fisheries. These management systems focus on regulating fishing effort, but in coastal ecosystems activities that change or destruct key habitats may have a greater effect on population abundance than does fishing mortality. The Golfo Artabro was analysed as a representative example of a coastal ecosystem in Galicia, and the spider crab Maja squinado used as a model of an exploited coastal invertebrate, for which shallow coastal areas are key habitats for juvenile stages. The commercial legal gillnet fishery for the spider crab harvests adults during their reproductive migrations to deep waters and in their wintering habitats. Illegal fisheries operate in shallow waters. The annual rate of exploitation is >90%, and <10% of the primiparous females reproduce effectively at least once. A simple spatially-explicit cohort model was constructed to simulate the population dynamics of spider crab females. Yield- and egg-per-recruit analyses corresponding to different exploitation regimes were performed to compare management policies directed to control the fishing effort or to protect key habitats. It was found that the protection of juvenile habitats could allow increases in yield and reproductive effort higher than in the present system, with such protection based in the control of the fishing effort of the legal fishery. Additionally, there is an urgent need for alternative research and management strategies in artisanal coastal fisheries based on the implementation of a system of territorial use rights for fishers, the integration of the fishers into assessment and management processes, and the protection of key habitats (marine reserves) as a basic tool for the regulation of the fisheries.

Feeding of the spider crab Maja squinado in rocky subtidal areas of the Ría de Arousa (north-west Spain)

The diet of the spider crab, Maja squinado, was studied in the rocky subtidal areas of the R|¤a de Arousa (Galicia, north-west Spain), by analysing the gut contents of crabs caught in the summer and winter of 1992. The highly diverse diet was made up primarily of macroalgae and benthic invertebrates that were either sessile or had little mobility.The most important prey were the seaweeds Laminariaceae (43% of the frequency of occurrence and15% of the food dry weight), Corallina spp. (38% and 3%), molluscs [the chiton Acanthochitona crinitus (15% and1%), the gastropods Bittium sp. (30% and 2%),Trochiidae and others andthe bivalve Mytilus sp. (32% and12%)], echinoderms [the holothurian Aslialefevrei (32% and18%) andthe echinoid Paracentrotus lividus (16% and 7%)] and solitary ascidians (18% and 6%). The variability in diet composition was determined by the season (Laminariaceae, Corallina spp., P. lividus, Mytilus sp., gastropods and chitons appeared in greater frequency in winter, while the solitary ascidians and A. lefevrei were consumedto a greaterextent in summer) inadditionto sexual maturity (prey such as Bittium sp. orTrochiidae were more common in juveniles). Moreover, the changes in the food consumption rate were linked primarily to the moult stage. Feeding activity plummeted during the phases immediately preceding and following ecdysis (stages D0^D3^4 and A), andthe diet was less diverse during these phases. No feeding diierences were found that could be linked to sex.The composition of the diet of Maja squinado appears to be determined by the seasonal abundance of the diierent prey in subtidal rocky areas and by their availability (depending on their behavioural and anatomical characteristics, mainly mobility and the presence of hard external structures). Moreover, life history factors have little importance in the variability of the diet composition and only the moultcyclehas a considerable eiecton feeding rate.

Movement patterns and habitat utilization in the spider crab Maja squinado (Herbst) (Decapoda, Majidae) measured by ultrasonic telemetry

Using ultrasonic telemetry, the activity and movement patterns (speed, distance and direction), and habitat utilization (depth, substratum) have been analyzed in juveniles approaching maturity and adults of the spider crab Maja squinado in the Ria de Arousa (Galicia, NW Spain). In summer three juveniles were tracked during a 23-day period and in winter five juveniles were tracked for 56 days in shallow rocky kelp forests (< 10 m), located in the outer area of the Ria. The juveniles showed a similar behaviour in both experiments, carrying out non-directional movements in restricted areas. No habitat changes were observed during the study period. Movement speed was slow in summer and winter (9.7 and 4.5 m/day, respectively), and the depths at which the animals were located also showed little variation (4.1 and 4.8 m). Seven adults were released in shallow zones, where they carried out the pubertal moult in summer; they were located in kelp beds, similar to those occupied by the juveniles, for an average of 53 days after release. During this first phase, adults showed a slightly higher speed (22.1 m/day) and depth (7.3 m) than juveniles, although there was no significant orientation observed in their movements. In late summer and in autumn adults began highly directional movements, oriented to the deeper zones (up to 40 m) in the outer and central channel of the Ria, with speeds averaging 76 m/day. This change in behaviour is linked to changes in meteorological conditions (changes in the direction of the prevailing winds and the beginning of a period of heavy rainfall) as well as oceanographic variations (a drop in the temperature and salinity of the shallow waters). The start of this migration may be related to the search for deeper waters which are more stable and suitable for the development of the reproductive processes.

Size at maturity of Liocarcinus depurator (Brachyura: Portunidae): a reproductive and morphometric study

Sexual maturity in brachyurans is often associated with an allometric change in the relative growth of the animal. Maturity of Liocarcinus depurator was examined by analysing the monthly percentages of mature females (determined by the stage of gonad maturation and the presence of brood and sperm plugs) by size-class and the relative growth of different body parts: length and width of the carapace, length, height and width of the cheliped propodus; width of the abdominal segments in females and length of the first pleopod in males. Using the reproductive criteria the size at the onset of sexual maturity (carapace width at which 50% females are mature) in females of L. depurator is around 30–34 mm cephalothorax width. Principal component analysis (PCA) showed that the main source of morphometric variation for both sexes was due to heterochelia and allometric changes in growth. Morphometric variables were fitted using different regression techniques to one and two-phase growth models. The length of the first pleopod and the propodus of the right cheliped in males, and width of abdominal segments in females showed two clearly differentiated phases. Estimated maturity size (carapace width) corresponding to 50% mature animals was greater in males than in females. In males, size at the onset of maturity ranged between 31.4 and 35.7 mm, depending on the methods and variables used. The size at the onset of maturity in females ranged between 25.5 and 31.5 mm. In the Ria de Arousa, the size at maturity in females of L. depurator estimated using reproductive criteria is considerably greater than the size found based on morphometric criteria. The size at maturity based on morphometric criteria is greater in males than in females.

MIGRATORY PATTERNS OF FEMALE SPIDER CRABS MAJA SQUINADO DETECTED USING ELECTRONIC TAGS AND TELEMETRY

Abstract Migrations play a key role in the life history of the spider crab Maja squinado (Herbst, 1788) and affect fishery catches. Migrations involve important changes in depth and in the environment. Ultrasonic telemetry has a number of drawbacks due to the difficulties in the continuous tracking of crabs while they are moving to deep waters. The recent introduction of electronic data storage or archival tags permits continuous monitoring of depth and temperature in crabs habitat and reconstruction of the movement patterns using baseline data on habitat characteristics. On the Galician coast (NW Spain) we calibrated and used electronic tags as a tool to study spider crab migrations. In the summer of 1996, 17 crabs were tagged with both ultrasonic transmitters and electronic tags. Tracking was carried out discontinuously at intervals of approximately 1 wk. We obtained a recapture rate of approximately 70%. The information provided by telemetry and electronic tags indicates autumn migrations along the bathymetric gradients (from <10 m down to 100 m) within short periods (mean = 5.7 d, range = 1.3–13.6). During these movements crabs travel through habitats characterized by different temperatures and substrates. Bathymetric and oceanographic data as well as localisation records from the electronic tags make the reconstruction of the animal tracks possible.

Geostatistical analysis of spatial distribution of Liocarcinus depurator, Macropipus tuberculatus and Polybius henslowii (Crustacea: Brachyura) over the Galician continental shelf (NW Spain)

Geostatistics was used to analyze the spatial structure and distribution of three species of brachyurans, Liocarcinus depurator, Macropipus tuberculatus and Polybius henslowii, from sets of data collected during three survey cruises (1983 and 1984) over the Galician continental shelf. The present study investigates the feasibility of using geostatistics with data collected according to traditional methods and of thereby improving the sampling methodology. In order to investigate the spatial structure of the species studied, experimental variograms were calculated and fitted to a spherical model. The spatial structure model was used to estimate and map abundance and distribution of the populations studied using the so-called “Kriging” technique. Geostatistical analysis enabled the determination of spatial density gradients as well as patch size (14 to 22 km, L. depurator; 10 to 28 km, M. tuberculatus; 7.5 to 28 km, P. henslowii) along the continental shelf. Depth was revealed as a limiting factor, restricting the distribution of L. depurator and M. tuberculatus on a large scale, whereas upwelling processes and nutrient-rich waters from the rías affected the spatial structure on a smaller scale, especially in the case of P. henslowii. A spatial segregation in the distribution of the three species also emerged; this probably arose from differences in physical and biological factors that result in different habitat-exploitation patterns. The study demonstrates the existence of spatial covariance and that the variograms vary as a function of population density and geographical area. This information will be useful in improving the design of future sampling cruises.

New approaches to the behavioural ecology of decapod crustaceans using telemetry and electronic tags

Decapod crustaceans have complex life histories and behaviour in aspects such as foraging, mating and reproduction, moulting and growth, habitat selection and migration. New technologies have enabled us to use an individual, field-based approach to analyze these problems, although they have been less developed in decapods than in marine vertebrates. These new possibilities are discussed here mainly from a biological point of view. There is a brief review of previous applications of telemetry to analyze habitat selection, foraging behaviour, energetics, moulting site selection and migrations in decapods, and two case studies are discussed in more detail. The first one refers to the study of differences in habitat use and movement patterns in juveniles and adults of coastal species that show ontogenetic habitat shifts, related to differences in selective pressures affecting both life history stages (predation risk, and growth and reproduction optimization). The second case study is dedicated to the migratory patterns in spider crabs combining telemetry and electronic tags. Operational limitations in tracking make it impossible to get detailed information on movement patterns during migration, which in turn involve an important bathymetric gradient and a change in the oceanographic environment (mainly temperature). Monitoring depth and temperature in the immediate habitat of the animals, using electronic data storage tags recovered by the fishery, allow for movement patterns to be modeled using supplementary information on the topography and hydrography of the study area. This approach is being tested using both telemetry and electronic tags simultaneously.