Growing reared spider crabs (Maja squinado) to sexual maturity: The first empirical data and a predictive growth model
Introduction
Spider crab fisheries are well developed in many European countries, with annual catches of 6299 tonnes according to the FAO (2010). The Mediterranean spider crab Maja squinado is one of the largest and most valued European species. This species was abundant 50 years ago in the Spanish Mediterranean. Currently, it is scarce (Abad, 2003) and considered endangered (UNEP, 1996) or even extinct (e.g., Mallorca Island; García, 2007).
Environmental degradation and inappropriate fishery management are the most common causes of the decline and even the collapse of certain fisheries (Born et al., 2004). Stocking (releasing cultured individuals) is one of the conventional options for allowing depleted stocks to recover and for managing fisheries (Blankenship and Leber, 1995). However, stocking has been criticized because it may be neither effective nor economically viable. The limited usefulness of stocking has been attributed to the tendency of cultured marine species to show lower survival, growth rate, reproductive fitness, and genetic diversity than wild individuals (Araki and Schmid, 2010, Bartley, 1996). Additional adverse consequences of releasing cultured individuals include ecological competition with wild individuals, genetic introgression or the spread of diseases (Bell et al., 2008, Frankham et al., 2002, Kostow, 2009, Lorenzen et al., 2012). However, positive effects have also been widely demonstrated, such as the enhancement of population abundance after stocking (Blanco Gonzalez et al., 2008a, Blanco Gonzalez et al., 2008b). At least two species of crabs have shown some stock enhancement after stocking: the swimming crab Portunus trituberculatus (Ariyama, 2001, Hamasaki et al., 2011) and the blue crab Callinectes sapidus (Zohar et al., 2008). It has also been reported that in some cases released hatchery-reared individuals do not harm wild stocks (Blanco González and Umino, 2009, Blanco Gonzalez et al., 2008a, Blanco Gonzalez et al., 2008b, Jeong et al., 2007). In addition, certain restocking programs, such as that for the Japanese flounder, have been proven economically viable (Kitada, 1999, Kitada and Kishino, 2006). Moreover, restocking programs have been proven useful for preserving endangered species, such as the beluga sturgeon (Abdolhay, 2004, Ivanov et al., 1997).
The Mediterranean spider crab may be a candidate for a stock enhancement program (Durán et al., 2012). However, a number of preliminary studies must be completed prior to launching such a program to circumvent the potential problems listed above. Specifically, to allow a sustainable population to recover, the survival probability must be sufficiently large to allow some of the released crabs to reach sexual maturity and to reproduce in the wild. Thus, the accurate knowledge of the growth rate and of the size and age at sexual maturity is very important. Unfortunately, despite the increasing interest in developing growth models and in determining the factors affecting growth and sexual maturation, crustacean growth is a very challenging topic (Chen and Kennelly, 1999, Verdoit et al., 1999). Crustaceans lack a structure comparable to the otolith in fish, and the molting process precludes long-term marking. Therefore, growth is only well known for a few species, including the Alaskan king crab Paralithodes camtschatica (McCaughran and Powel, 1977), the American lobster Homarus americanus (Fogarty and Idoine, 1988), the Dungeness crab Cancer magister (Wainwright and Armstrong, 1993) and the blue crab C. sapidus (Brylawski and Miller, 2006). The patterns of growth are not well known for M. squinado. For this commercially important and endangered species, only the data on early juvenile growth have been reported (Guerao and Rotllant, 2010). However, no data are available from this early juvenile stage to sexual maturity for neither wild nor cultured individuals, and the only additional information available involves general biological traits and is based on data from commercial landings (Stevcic, 1963, Stevcic, 1968, Stevcic, 1971, Stevcic, 1973, Stevcic, 1976).
This paper reports the first successful occurrence of mating in the laboratory involving laboratory-born and laboratory-reared specimens of M. squinado. Egg masses and viable zoeae were obtained from these matings. This evidence demonstrates that the entire life cycle of the Mediterranean spider crab was completed in captivity. We report the first successful attempt to grow M. squinado from larvae to sexual maturity, and present the first growth data on individually monitored M. squinado to the age of sexual maturity. In addition, we have developed a growth model that incorporates the molting probability as a function of the temperature and the pre-molt size. This model has been coupled with a size-dependent model for predicting the molting increment and sexual maturity. Despite the use of individuals raised in aquaculture to parameterize the model, the data and model presented in this paper will be useful for managing the ongoing stocking program for M. squinado in the Balearic Islands (Durán et al., 2012), thus opening new opportunities for aquaculture to shift from an exclusive role in biomass production to an alternative approach to the sustainable management of stocks.
Section snippets
Materials and methods
Viable zoeae were obtained in the laboratory (Laboratori d'Investigacions Marines i Aqüicultura, LIMIA, Port d'Andratx, Mallorca) from wild female crabs in 2008, 2009 and 2010. First-instar juvenile crabs (C1) were reared together in mass culture tanks for 150–210 days. Subsequently, they were individually monitored until they were nearly 500 days old.
Results
The number of molts monitored per crab ranged from one to nine molts for both sexes. After a few outliers were removed from the data, 102 observations of MI and 75 observations of IP from 30 females (22 with more than one controlled molt) and 81 observations of MI and 62 observations of IP from 25 males (17 with more than one controlled molt) were considered for further analysis. The raw data (length and age of molts) are provided as Supplementary material.
Discussion
This paper reports the first successful occurrence of mating in the laboratory involving laboratory-born and laboratory-reared specimens of M. squinado. Egg masses and viable zoeae were obtained from these matings. This evidence demonstrates that the entire life cycle of the Mediterranean spider crab was completed in captivity. In addition, we present the first growth data on individually monitored M. squinado to the age of sexual maturity. We reported a long time series of high-quality
Acknowledgments
Financial support was provided by JACUMAR (“Cultivo de la centolla” and “Propuestas y mejoras para el diseño de los planes de repoblación y evaluación del impacto de los escapes” projects) and by the Government of the Balearic Islands. We are especially grateful to Dr. Amalia Grau for her help in histological observations and to the laboratory technicians, scholars and trainees at LIMIA for their help and support on the development of this study. Particular thanks go to three anonymous
References (92)
- et al.
Individual variability and sex-related differences in the growth of Diplodus annularis (Linnaeus, 1758)
Fisheries Research
(2010) - et al.
Is hatchery stocking a help or harm? Evidence, limitations and future directions in ecological and genetic surveys
Aquaculture
(2010) - et al.
Morphological conditioning of a hatchery-raised invertebrate, Callinectes sapidus, to improve field survivorship after release
Aquaculture
(2005) - et al.
Growth at moult and moulting seasonality of the spider crab, Maja squinado (Herbst) (Decapoda: Majidae) in experimental conditions: implications for juvenile life history
Journal of Experimental Marine Biology and Ecology
(1995) - et al.
Survival and growth of post-settlement juveniles of the spider crab Maja brachydactyla (Brachyura: Majoidea) reared under individual culture system
Aquaculture
(2009) - et al.
Development and growth of the early juveniles of the spider crab Maja squinado (Brachyura, Majidae) in an individual culture system
Aquaculture
(2010) - et al.
Growth to maturity of juveniles of the spider crabs Hyas coarctatus Leach and Inachus dorsettensis (Pennant) (Brachyura: Majidae)
Journal of Experimental Marine Biology and Ecology
(2001) - et al.
Lessons learned from Japanese marine finfish stock enhancement programmes
Fisheries Research
(2006) - et al.
Ecdysteroids and juvenoids in two male morphotypes of Libinia emarginata
Insect Biochemistry and Molecular Biology
(1993) - et al.
Cannibal-prey dynamics in juveniles and postlarvae of the blue crab
Journal of Experimental Marine Biology and Ecology
(1997)
Modelling survival and growth of Mithraculus forceps larvae and juveniles (A. Milne Edwards, 1875) (Decapoda: Brachyura: Majidae) in aquaculture
Aquaculture
Growth, development, and survival of larval Mithraculus sculptus (Lamark) and Mithraculus forceps (A. Milne Edwards) (Decapoda: Brachyura: Majidae): economically important marine ornamental crabs
Aquaculture
Role of ecdysteroids and methyl farnesoate in morphogenesis and terminal moult in polymorphic males of the spider crab Libinia emarginata
Aquaculture
Methyl farnesoate levels in male spider crabs exhibiting active reproductive behavior
Hormones and Behavior
Large-scale juvenile production of the blue crab Callinectes sapidus
Aquaculture
Actas de las I Jornadas sobre Reservas Marinas y I Reunión de la Red Iberoamericana de Reservas Marinas (RIRM)
Sturgeon stocking programme in the Caspian Sea with emphasis on Iran. Marine ranching
How to enhance the stock of swimming crab Portunus trituberculatus by release of juveniles
Conservation of biological diversity in hatchery enhancement programmes
A new era for restocking, stock enhancement and sea ranching of coastal fisheries resources
Reviews in Fisheries Science
Fine-scale genetic structure derived from stocking black sea bream, Acanthopagrus schlegelii (Bleeker, 1854), in Hiroshima Bay, Japan
Journal of Applied Ichthyology
Stock enhancement program for black sea bream (Acanthopagrus schlegelii) in Hiroshima Bay: monitoring the genetic effects
Aquaculture
Stock enhancement programme for black sea bream, Acanthopagrus schlegelii (Bleeker), in Hiroshima Bay, Japan: a review
Aquaculture Research
A responsible approach to marine stock enhancement
Uses and Effects of Cultured Fishes in Aquatic Ecosystems
American Fisheries Society Symposium
Marine and coastal stocking: global status and information needs. Marine ranching
Studies on the Biology, Ecology and Fishery of the Spider Crab Maja squinado Herbst (1788) off the West Coast of Ireland
Temperature-dependent growth of the blue crab (Callinectes sapidus), a molt process approach
Canadian Journal of Fisheries and Aquatic Sciences
Growth of spanner crabs, Ranina ranina, off the east coast of Australia
Marine and Freshwater Research
Determinants of postmolt size in the American lobster (Homarus americanus). I. D13 is the critical stage
Canadian Journal of Fisheries and Aquatic Sciences
Functional maturity and terminal molt of male snow crab, Chionoecetes opilio
Canadian Journal of Fisheries and Aquatic Sciences
Review of literature on life histories in the genus Chionoecetes in light of recent findings on growth and maturity of C. opilio in Eastern Canada
Morphometric and gonad maturity in the spider crab Maja brachydactyla: a comparison of methods for estimating size at maturity in species with determinate growth
Journal of Marine Science
Male dominance hierarchy and mating tactics in the rock shrimp Rhynchocinetes typus (Decapoda: Caridea)
Journal of Crustacean Biology
Reproductive Performance of Orange Mud Crab
Scylla olivacea (Herbst), Broodstock Fed Selected Foods
Mue et cycle d'intermue chez les crustacés décapodes
Annales de l'Institut Océanographique Mónaco
Cultivo larvario de la centolla mediterránea, Maja squinado, usando diferentes secuencias alimenticias
First results of embryonic development, spawning and larval rearing of the Mediterranean spider crab Maja squinado (Herbst 1788) under laboratory conditions, a candidate species for a restocking program
Aquaculture Research
FAO Yearbook. Fishery and Aquaculture Statistics, Catches and Landings
Application of a yield per recruit and egg production model based on size to an offshore American lobster population
Transactions of the American Fisheries Society
Introduction to Conservation Genetics
Reproductive biology of spider crab females (Maja brachydactyla) off the coast of Asturias (North-West Spain)
Journal of the Marine Biological Association of the United Kingdom
Maturity in male stone crab Hapalogaster dentata (Anomura: Lithodidae) and its application for fishery management
Journal of Crustacean Biology
Effect of salinity on survival and bioenergetics of juvenile lesser blue crabs, Callinectes similis
Marine Biology
A review of seed production and stock enhancement for commercially important portunid crabs in Japan
Aquaculture International
The biology of Manx spider crabs
Proceedings Zoological Society of London
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