Marine Biology

, Volume 152, Issue 2, pp 383–394 | Cite as

Ovarian maturation of the multi-spawning spider crab Maja brachydactyla (Decapoda: Majidae) with special reference to yolk formation

  • Guiomar RotllantEmail author
  • Eduardo González-Gurriarán
  • Luis Fernández
  • Khadra Benhalima
  • Enric Ribes
Research Article


In the study of the reproductive biology of the spider crab Maja brachydactyla, the morphology of the female reproductive system and yolk formation have long been overlooked. Females spawn two or three times during their annual reproductive cycle in northern Spain (Galicia). The ovaries consist of two lobes. The right and left lobes are connected by a small cross-lobe at the level of the heart and merge at the posterior edge. Before merging, the ovaries descend to the ventral part of the body, joining the spermathecae in the vagina, which opens through a chitin tube to the gonopore, located in the sternite, at the level of the third walking leg. No morphological changes have been observed between either the different parts of the ovaries or the different annual spawning periods. At the start of vitellogenesis, the oocyte of M. brachydactyla is characterized by a large number of vesicles in the cytoplasm. These vesicles are surrounded by a unit membrane whose size increases as the oocyte matures and contain fine granular material including a variable number of ovoid, electron-dense granules. The vesicles are of diverse origin, although most of them develop directly from the mitochondria and the Golgi complex (endogenous phase of vitellogenesis). In a subsequent phase, a series of substances (principally lipoproteins) are incorporated into the ooplasma by means of micropinocytosis. These substances are also involved in yolk formation (exogenous phase of vitellogenesis). During vitellogenesis in M. brachydactyla, mitochondria play the most important role since they are not only the energetic centre of the cellule, but they also act as containers of high-energy reserve substances: the yolk granules.


Crab Species Yolk Granule Spider Crab Germinal Zone Galician Coast 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Support for this work was provided by several projects from the Consellería de Pesca, Marisqueo e Acuicultura of the Xunta de Galicia (PE608A 94/2-0 among others), the Spanish DGICYT project (PB94-0501), the Spanish CICYT Projects (MAR97-0446 and REN2001-0729) and the Centre de Referència en Aqüicultura of the Catalan Government.


  1. Adiyodi RG, Subramoniam T (1983) Arthropoda—Crustacea. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol I: oogenesis, oviposition, and oosorption. Wiley, New York, pp 443–495Google Scholar
  2. Anderson E (1964) Oocyte differentiation and vitellogenesis in the roach Periplaneta americana. J Cell Biol 20:131–155CrossRefGoogle Scholar
  3. Ando H, Makioka T (1999) Structure of the ovary and mode of oogenesis in a freshwater crab Potamon dehaani. J Morphol 239:107–114CrossRefGoogle Scholar
  4. Andre J (1962) Contribution à la connaissance du chondriome. Ètude de ses modificacions ultraestructurales pendant la spermatogenèse. J Ultrastruct Res Suppl 3:1–185CrossRefGoogle Scholar
  5. Arnaud J, Brunet M, Mazza J (1982) Ètude de l’ovogenèse chez Centropages typicus. (Copepoda, Calanoida). Reprod Nutr Dév 22(3):537–555CrossRefGoogle Scholar
  6. Azevedo C, Coimbra A (1980) Evolution of nucleoli in the course of oogenesis in a viviparous teleost (Xiphophorus helleri). Biol Cell 38:43–48Google Scholar
  7. Beams HW, Kessel RG (1963) Electron microscope studies on developing crayfish oocytes with special references to the origin of yolk. J Cell Biol 18:621–649CrossRefGoogle Scholar
  8. Beams HW, Kessel RG (1980) Ultrastructure and vitellogenesis in the oocyte of the crustacean, Oniscus asellus. J Submicrosc Cytol 12:17–27Google Scholar
  9. Beninger PG, Lanteigne C, Elner RW (1993) Reproductive processes revealed by spermatophore dehiscence experiments and by histology, ultrastructure, and histochemistry of the female reproductive system in the snow crab Chionoecetes opilio (O. Fabricius). J Crustacean Biol 13(1):1–16CrossRefGoogle Scholar
  10. Blades-Eckelbarger PI, Youngbluth MJ (1984) The ultrastructure of oogenesis and yolk formation in Labidocera aestiva (Copepoda: Calanoida). J Morphol 179:33–46CrossRefGoogle Scholar
  11. Brosnan DM (1981) Studies on the biology, ecology and fishery of the spider crab Maia squinado Herbst (1768) of the west coast or Ireland. PhD thesis, University College, Galway, pp 133Google Scholar
  12. Brownell WN, Provenzano Jr AJ, Matinez M (1977) Culture of the West Indian spider crab (Mithrax spinosissimus) at Los Roques, Venezuela. Proc World Maricult Soc 8:157–168CrossRefGoogle Scholar
  13. Chiba A, Honma Y (1972) Studies on gonad maturity in some marine invertebrates. 7. Seasonal changes in the ovary of the lined shore crab. Bull Jpn Soc Sci Fish 38:323–327CrossRefGoogle Scholar
  14. Clerot JC (1968) Mise en evidence par cytochimie ultrastructurale de l’émision de protéines par le noyau d’auxocytes de Batraciens. J Microscopie 7:973–992Google Scholar
  15. Clerot JC (1976) Les groupements mitochondriaux des cellules germinales des poissons Téléostéens Cyprinidés. I. Ètude ultrastructurale. J Ultrastruct Res 54:461–475CrossRefGoogle Scholar
  16. Clotilde-Ba FL, Diatta Y, Capapé C (1997) Observations sur huit espèces comestibles de crustacés décapodes des eaux sénégalaises (Afrique de l’ouest). Bol Mus Mun Funchal 49(282):171–187Google Scholar
  17. Dhainaut A, De Leersnyder M (1976) Etude cytochimique et ultrastructurale de l’evolution ovocitaire du crabe Eriocheir sinensis. I. Ovogenèse naturelle. Arch Biol 87:261–282Google Scholar
  18. Diesel R (1991) Sperm competition and the evolution of mating behavior in Brachyura, with special reference to spider crabs (Decapoda: Majidae). In: Martin RGB, Martin JW (eds) Crustacean sexual biology. University Press, New York, pp 145–163Google Scholar
  19. Eddy EM (1975) Germ plasm and the differentiation of the germ cell line. In: Bourne GH, Danielli JF (eds) International review of cytology, vol 43. Academic, New York, pp 229–280Google Scholar
  20. Edwards E (1979) Preliminary results of an investigation on a new fishery for spider crabs (Maia squinado) along the south coast of England. ICES Shellfish Committee CM 1979/K14 9ppGoogle Scholar
  21. Elner RW, Beninger PG (1992) The reproductive biology of snow crab, Chionoecetes opilio: a synthesis of recent contributions. Am Zool 32:524–533CrossRefGoogle Scholar
  22. Eurenius L (1973) An electron microscope study on the developing oocytes of the crab Cancer pagurus L. with special reference to yolk formation (Crustacea). Z Morph Tiere 75:243–254CrossRefGoogle Scholar
  23. Fernández-Vergaz V, López Abellán JL, Balguerías E (2000) Morphometric, functional and sexual maturity of the deep-sea red crab Chaceon affinis inhabiting Canary Island waters: chronology of maturation. Mar Ecol Prog Ser 204:169–178CrossRefGoogle Scholar
  24. García Cabrera C (1972) Estudio biológico pesquero del Centollo en aguas del litoral sahariano. Bol Inst Esp Oceanogr 156:1–36Google Scholar
  25. García-Flórez L, Fernández-Rueda P (2000) Reproductive biology of spider crab females (Maja brachydactyla) off the coast of Asturias (north-west Spain). J Mar Biol Assoc UK 80:1071–1076CrossRefGoogle Scholar
  26. Goldstein J, Newbury D, Joy D, Lyman Ch, Echlin P, Litshin E, Sawyer L, Michael J (2003) Scanning electron microscopy and x-ray microanalysis, 3rd edn. Kluwer Academic/Plenum Publishers, New York, pp 647–673Google Scholar
  27. González-Gurriarán E, Fernández L, Freire J, Muiño R (1993) Reproduction of the spider crab Maja squinado (Brachyura: Majidae) in the southern Galician coast (NW Spain). ICES:15ppGoogle Scholar
  28. González-Gurriarán E, Freire J, Parapar J, Sampedro MP, Urcera M (1995) Growth at moult and moulting seasonality of the spider crab, Maja squinado (Herbst) (Decapoda: Majidae) in experimental conditions: implications for juvenile life history. J Exp Mar Biol Ecol 189:183–203CrossRefGoogle Scholar
  29. González-Gurriarán E, Fernández L, Freire J, Muiño R (1998) Mating and role of seminal receptacles in the reproductive biology of the spider crab Maja squinado (Decapoda: Majidae). J Exp Mar Biol Ecol 220:269–285CrossRefGoogle Scholar
  30. González-Gurriarán E, Freire J, Bernárdez C (2002) Migratory patterns of female spider crabs Maja squinado detected using electronic tags and telemetry. J Crustacean Biol 22(1):91–97CrossRefGoogle Scholar
  31. Hamasaki K, Imai H, Akiyama N, Fukunaga K (2004) Ovarian development and induced oviposition of the overwintering swimming crab Portunus trituberculatus (Brachyura: Portunidae) reared in the laboratory. Fish Sci 70:988–995CrossRefGoogle Scholar
  32. Hartnoll RG (1965) The biology of spider crabs: a comparison of British and Jamaican species. Crustaceana 9:1–16CrossRefGoogle Scholar
  33. Hartnoll RG (1968) Morphology of the genital ducts in female crabs. J Linn Soc (Zool) 47:279–300CrossRefGoogle Scholar
  34. Hartnoll RG (1969) “Mating in the brachyura.” Crustaceana 16:161–181CrossRefGoogle Scholar
  35. Hinsch GW (1992) Ovary of the golden crab, Chaceon fenneri: post-spawning and oosorption. J Morphol 211:1–6CrossRefGoogle Scholar
  36. Hinsch GW, Cone V (1969) Ultrastructural observations of vitellogenesis in the spider crab, Libinia emarginata L. J Cell Biol 40:336–342CrossRefGoogle Scholar
  37. Hoestlandt H (1948) Recherches sur la biologie de l’Eriocheir sinensis H. Milne-Edwards (crustacé brachyoure). Ann Inst Ocean 24:1–116Google Scholar
  38. Hubert J (1972) Ultrastructure du nucleoli au cours du stade diplotène dans les ovocytes du Lézard Lacerta vivipara. Jacquin Arch Anat Microsc 61(4):325–338Google Scholar
  39. Iglesias J, Sánchez FJ, Moxica C, Fuentes L, Otero JJ, Pérez JL (2002) Datos preliminares sobre el cultivo de larvas y juveniles de centolla Maja squinado Herbst, 1788 en el Centro Oceanográfico de Vigo del Instituto Español de Oceanografía. Bol Inst Esp Oceanogr 18(1–4):25–30Google Scholar
  40. Jensen PC, Orensanz JM, Amstrong DA (1996) Structure of the female reproductive tract in the dungeness crab (Cancer magister) and implications for the mating system. Biol Bull 190:336–349CrossRefGoogle Scholar
  41. Kalt MR (1973) Ultrastructural observations on the germ line of Xenopus laevis. Zeits Zellforsch 138:41–62CrossRefGoogle Scholar
  42. Karnovsky MJ (1965) A formaldehyde–glutaldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138Google Scholar
  43. Kergariou G (1971) L’araignee de mer, Maia squinado L., sur le littoral de Bretagne. Bull Inst Pêches Marit 205:11–19Google Scholar
  44. Kergariou G (1975) Contribution à l’étude de la reproduction de l’ araignée de mer, (Maja squinado H.). ICES, Shellfish and Benthos Committee CM 1975/K:34 8ppGoogle Scholar
  45. Kessel RG (1968) Fine structure of annulate lamellae. J Cell Biol 36:658–664CrossRefGoogle Scholar
  46. Kessel RG (1968) Mechanism of protein yolk synthesis and deposition in Crustacean oocytes. Z Zellfrorsch Mikrosk Anat 89:17–38CrossRefGoogle Scholar
  47. Kon T, Honma Y (1970a) Studies on the maturity of the gonad in some marine invertebrates-III. Seasonal changes in the ovary of the tanner crab. Bull Jpn Soc Sci Fish 36(10):1021–1027CrossRefGoogle Scholar
  48. Kon T, Honma Y (1970b) Studies on the maturity of the gonad in some marine invertebrates -IV. Seasonal changes in the testes of the tanner crab. Bull Jpn Soc Sci Fish 36(10):1028–1033CrossRefGoogle Scholar
  49. Lanteigne C, Beninger PG, Gionet C (1996) Ontogeny of female primary sexual characters in the majid crabs Chionoecetes opilio and Hyas coarctatus. J Crustacean Biol 16(3):501–514CrossRefGoogle Scholar
  50. Le Foll D (1993) Biologie et exploitation de l’araignée de mer Maja squinado Herbst en Manche Ouest. PhD thesis, Université de Bretagne Occidentale, IFREMER, 524ppGoogle Scholar
  51. López-Abellán LJ, Balguerías E, Fernández-Vergaz V (2002) Life history characteristics of the deep-sea crab Chaceon affins population off Tenerife (Canary Islands). Fish Res 58:231–239CrossRefGoogle Scholar
  52. Martoja R, Martoja M (1967) Initiations aux techniques de l’histologie animale. Masson et Cie, Paris, pp 350Google Scholar
  53. Meusy JJ, Payen GG (1988) Female reproduction in Malacostracan crustacean. Zool Sci 5:217–265Google Scholar
  54. Meyer CG (1993) The biology and fishery of the spider crab (Maja squinado) around Jersey (Channel Islands).PhD thesis, University of Plymouth, Plymouth, 116ppGoogle Scholar
  55. Minagawa M, Chiu JR, Kudo M, Ito E, Takashima F (1993) Female reproductive biology and oocyte development of the red frog crab, Ranina ranina, off Hachijojima, Izu Islands, Japan. Mar Biol 115:613–623CrossRefGoogle Scholar
  56. Newman V (1998) A review of the Maja squinado (Crustacea: Decapoda: Brachyura) species-complex with a key to the eastern Atlantic and Mediterranean species of the genus. J Natl Hist 32:1667–1684CrossRefGoogle Scholar
  57. Pochon-Masson J (1994) Les Gamétogenèses. In: Forest J (ed) Traité de Zoologie Pierre-P Grassé, vol VII: Crustacés, Fascicule I: Morphologie, Physiologie, Reproduction, Systématique. Masson, Paris-Milan-Barcelona, pp 727–783Google Scholar
  58. Pradeille-Rouquette M (1975) Étude de la fonction de reproduction chez les femelles du crabe Pachygrapsus marmoratus (F.) et de différents facteurs qui lui sont liés (I). Cah Biol Mar 17:387–403Google Scholar
  59. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212CrossRefGoogle Scholar
  60. Rodhouse DM (1984) Experimental fishing for the spider crab, Maia squinado: sea and laboratory trials. J Mar Biol Assoc UK 64:251–259CrossRefGoogle Scholar
  61. Ryan EP (1967) Structure and function of the reproductive system of the crab Portunus sanguinolentus (Herbst) (Brachyura: Portunidae) II. The female system. Proceedings of the Symposium on Crustacea. Mar Biol Assoc India Ernakulam. Part II: 522–544Google Scholar
  62. Sampedro MP, González-Gurriarán E, Freire J, Muiño R (1999) Morphometry and sexual maturity in the spider crab Maja squinado (Decapoda: Majidae) in Galicia, Spain. J Crustacean Biol 19(3):578–592CrossRefGoogle Scholar
  63. Sainte-Marie G, Sainte-Marie B (1998) Morphology of the spermatheca, oviduct, intermediate chamber, and vagina of the adult snow crab (Chionoecetes opilio). Can J Fish Aquat Sci 76:1589–1604Google Scholar
  64. Smith KD, Potter IC, Hesp SA (2004) Comparisons between the reproductive biology of females of two species of deep sea crabs that live in different water depths. J Shellfish Res 23(3):887–896Google Scholar
  65. Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 81:341–350Google Scholar
  66. Stevcic Z (1967) A short outline of the biology of the spinous spider crab. Bull Sci Conseil Acad RSF Yugoslavie Sect A 12:313–314Google Scholar
  67. Stevcic Z (1977) Contribution a la connaissance de la preoduction de l’araigné de mer (Maja squinado). Rapp Comm int Mer Medit 24:177–178Google Scholar
  68. Zerbib C (1979) Etude ultrastructurale de l’ovocyte en vitellogenèse chez les Ecrevisses Astacus astacus et Astacus leptodactilus. Int J Invert Reprod 1:289–295CrossRefGoogle Scholar
  69. Zerbib C (1980) Ultrastructural observation of oogenesis in the Crustacea Amphipoda Orchestia gammarelus (Pallas). Tissue Cell 12:47–62CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Guiomar Rotllant
    • 1
    Email author
  • Eduardo González-Gurriarán
    • 2
  • Luis Fernández
    • 2
  • Khadra Benhalima
    • 3
  • Enric Ribes
    • 4
  1. 1.IRTATarragonaSpain
  2. 2.Departamento de Bioloxía Animal, Bioloxía Vexetal e EcoloxíaUniversidade da CoruñaA CoruñaSpain
  3. 3.Department of Fisheries and Oceans, Invertebrate Fisheries Division, Science BranchMaritimes RegionMonctonCanada
  4. 4.Department of Cell Biology, Faculty of BiologyUniversity of BarcelonaBarcelonaSpain

Personalised recommendations