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Contrasting macroscopic maturity staging with histological characteristics of the gonads in female Octopus vulgaris

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Abstract

We contrasted histological characteristics with a macroscopic maturity scale in Octopus vulgaris. Seven histological stages of maturation were identified, and a stereological method was used to develop a new histological maturity index (HMI). This index was related to the gonadosomatic index giving the possibility to estimate the histological stage of individual octopus without sampling the gonads. However, the existing macroscopic maturity scale produced some degree of overlap along the range of HMI, suggesting that this macroscale at this moment might be just good enough to separate immature from fully mature individuals. A histological maturity criterion based on the presence of a larger proportion of folding oocytes compared to earlier microstages resulted in a size at maturity of 1.5 kg. However, using two different macroscopic criteria, size at maturity was 1.3 and 2.3 kg. The estimate of size at maturity is therefore sensitive to the maturity criteria used. The maturation cycle of female O. vulgaris was seasonal, peaking in spring months and reaching a maximum of reproductive activity in April independently of the maturation criteria used. Oogenesis was reviewed and found to be an asynchronic process. Our results suggest that there is a need to examine all these issues in other cephalopod species.

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References

  • Bolognari, A., M. P. A. Carmignani & G. Zaccone, 1976. A cytochemical analysis of the follicular cells and the yolk in the growing oocytes of Octopus vulgaris (cephalopoda, mollusca). Acta Histochemica 55: 167–175.

    Article  CAS  PubMed  Google Scholar 

  • Brown-Peterson, N., D. M. Wyanski, F. Saborido-Rey, B. J. Macewicz & S. Lowerre-Barbieri, 2011. A standardized terminology for describing reproductive development in fishes. Marine and Coastal Fisheries 3: 52–70.

    Article  Google Scholar 

  • Buckley, S. K. L., 1977. Oogenesis and Its Hormonal Control in Octopus vulgaris. Ph.D. Thesis, University of Cambridge, Cambridge.

  • Castro, B. G., J. L. Garrido & C. G. Sotelo, 1992. Changes in composition of digestive gland and mantle muscle of the cuttlefish Sepia officinalis during starvation. Marine Biology 114: 11–20.

    CAS  Google Scholar 

  • Cuccu, D., M. Mereu, C. Porcu, M. C. Follesa, A. L. Cau & A. Cau, 2013. Development of sexual organs and fecundity in Octopus vulgaris Cuvier, 1797 from the Sardinian waters (Mediterranean Sea). Mediterranean Marine Science 14: 270–277.

    Article  Google Scholar 

  • Delesse, M. A., 1847. Procédé mécanique pour déterminer la composition des roches. Comptes Rendus de l’Académie des Sciences 25: 544–545.

    Google Scholar 

  • Di Cosmo, A. D. & C. Di Cristo, 2001. Sex steroid hormone fluctuations and morphological changes of the reproductive system of the female of Octopus vulgaris throughout the annual cycle. Journal of Experimental Zoology 289: 33–47.

    Article  PubMed  Google Scholar 

  • Dia, M. & A. Goutschine, 1990. The sexual maturity scale of octopus (Octopus vulgaris, Cuvier 1797) of Mauritanian waters. Bulletin Scientifique du Centre National de Recherches Océanographiques et des Pêches 21: 1–6.

    Google Scholar 

  • Díaz-Uribe, J. G., A. Hernández-Herrera, E. Morales-Bojórquez, S. Martínez-Aguilar, M. C. Suárez-Higuera & A. Hernández-López, 2006. Histological validation of the gonadal maturation stages of female jumbo squid (Dosidicus gigas) in the Gulf of California, Mexico. Ciencias Marinas 32: 23–31.

    Google Scholar 

  • Domínguez-Petit, R., 2007. Study of reproductive potential of Merluccius merluccius in the Galician Shelf. Ph.D. Thesis, University of Vigo, Spain.

  • Estefanell, J., J. Socorro, F. J. Roo, R. Guirao, H. Fernández-Palacios & M. Izquierdo, 2010. Gonad maturation in Octopus vulgaris during ongrowing, under different conditions of sex ratio. ICES Journal of Marine Science 67: 1487–1493.

    Google Scholar 

  • Gabe, M., 1968. Techniques Histologiques. Masson et Cie Editeurs, Paris.

    Google Scholar 

  • Gonçalves, I., J. Sendão & T. C. Borges, 2002. Octopus vulgaris (Cephalopoda: Octopodidae) gametogenesis: a histological approach to the verification of the macroscopic maturity scales. Abhandlungen der Geologischen Bundesanstalt A 57: 79–88.

    Google Scholar 

  • Gonçalves, J. M., 1993. Octopus vulgaris Cuvier, 1797 (Polvo-Comum): Sinopse da Biologia e Exploração. Ph.D. Thesis, University of Açores, Portugal.

  • Guerra, A., 1975. Determinación de las diferentes fases de desarrollo sexual de Octopus vulgaris Lamarck, mediante un índice de madurez. Investigaciones Pesqueras 39: 397–416.

    Google Scholar 

  • Guerra, A., 2006. Estrategias evolutivas de los cefalópodos. Investigación y Ciencia 355: 50–59.

    Google Scholar 

  • Hernández-García, V., J. L. Hernández-López & J. J. Castro-Hernández, 2002. On the reproduction of Octopus vulgaris off the coast of the Canary Islands. Fisheries Research 57: 197–203.

    Article  Google Scholar 

  • Hoving, H. J. T., V. V. Laptikhovsky, M. R. Lipinski & E. Jürgens, 2013. Fecundity, oogenesis, and ovulation pattern of southern African Lycoteuthis lorigera (Steenstrup, 1875). Hydrobiologia. doi:10.1007/s10750-013-1586-6.

    Google Scholar 

  • ICES, 2010. Report of the Workshop on Sexual Maturity Staging of Cephalopods (WKMSCEPH) ICES CM 2010/ACOM 49, Livorno, Italy.

  • Idrissi, F. H., N. Koueta, M. Idhalla, D. Belghyti & S. Bencherifi, 2006. The modalities of the sexual cycle of Octopus vulgaris in the southern Moroccan Atlantic (Tantan, Boujdour). Comptes Rendus Biologies 329: 903–911.

    Article  Google Scholar 

  • Inejih, C. A. O., 2000. Dynamique Spatio-Temporelle et Biologie du Poulpe (Octopus vulgaris) dans les Eaux Mauritanienne: Modélisation de l’Abondance et Aménagement des Pêcheries. Ph.D. Thesis, Université de Bretagne Occidentale, France.

  • Jiménez-Badillo, M. L., R. E. Río-Rodríguez, M. I. Gómez-Solano, A. Cu-Escamilla & D. Méndez-Aguilar, 2008. Madurez Gonádica del Pulpo Octopus vulgaris en el Golfo de México: Análisis Macroscópico y Microscópico. Universidad Autónoma de Campeche, México. http://epomex.uacam.mx.

  • Khallahi, O. M. F., 2002. Étude de la gamétogenèse chez le poulpe Octopus vulgaris (Cuvier, 1797). Bulletin Scientifique du Centre National de Recherches Océanographiques et des Pêches 28: 44–52.

    Google Scholar 

  • Khallahi, O. M. F. & C. A. O. Inejih, 2002. Proposition d’une échelle macroscopique de maturité sexuelle des femelles de poulpe Octopus vulgaris (Cuvier, 1797). Bulletin Scientifique du Centre National de Recherches Océanographiques et des Pêches 23: 51–57.

    Google Scholar 

  • Lipinski, M. R. & G. Underhill, 1995. Sexual maturation in squid: quantum or continuum? South African Journal of Marine Science 15: 207–223.

    Article  Google Scholar 

  • Lourenço, S., A. Moreno, L. Narciso, A. F. González & J. Pereira, 2012. Seasonal trends of the reproductive cycle of Octopus vulgaris in two environmentally distinct coastal areas. Fisheries Research 127(128): 116–124.

    Article  Google Scholar 

  • Mangold, K., 1963. Biologie des Céphalopodes Benthiques et Nectoniques de la Mer Catalane. Vie et Milieu, supplément no. 13, Hermann, Banyuls-sur-Mer.

  • Marza, V., 1938. Histophysiologie de L’ovogenèse. Herman et Cie, Paris.

    Google Scholar 

  • Murua, H., G. Kraus, F. Saborido-Rey, P. R. Witthames & S. Junquera, 2003. Procedures to estimate fecundity of marine fish species in relation to their reproductive strategy. Journal of Northwest Atlantic Fishery Science 33: 33–54.

    Article  Google Scholar 

  • Nigmatullin, C. M., 2002. Ovary development, potential and actual fecundity and oocyte resorption in coleoid cephalopods: a review. Berliner Paläobiologische Abhandlungen 1: 82–84.

    Google Scholar 

  • Olivares Paz, A., M. Zamora, P. Portilla & O. Zuniga, 2001. Estudio histológico de la ovogénesis y maduración ovárica en Octopus mimus (Cephalopoda: Octopodidae) de la II Región de Chile. Estudios Oceanológicos 20: 13–22.

    Google Scholar 

  • Ortiz, N., 2013. Validation of macroscopic maturity stages of the Patagonian red octopus Enteroctopus megalocyathus. Journal of the Marine Biological Association of the United Kingdom 93: 833–842.

    Article  Google Scholar 

  • Otero, J., A. F. González, M. P. Sieiro & A. Guerra, 2007. Reproductive cycle and energy allocation of Octopus vulgaris in Galician waters, NE Atlantic. Fisheries Research 85: 122–129.

    Article  Google Scholar 

  • Pierce, G. J., L. Allcock, I. Bruno, P. Bustamante, A. González, A. Guerra, P. Jereb, E. Lefkaditou, S. Malham, A. Moreno et al., 2010. Cephalopod Biology and Fisheries in Europe. ICES Cooperative Research Report No. 303.

  • R Development Core Team, 2012. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org.

  • Rocha, F., A. Guerra & A. F. González, 2001. A review of reproductive strategies in cephalopods. Biological Reviews 76: 291–304.

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Rúa, A., I. Pozuelo, M. A. Prado, M. J. Gómez & M. A. Bruzón, 2005. The gametogenic cycle of Octopus vulgaris (Mollusca: Cephalopoda) as observed on the Atlantic coast of Andalusia (south of Spain). Marine Biology 147: 927–933.

    Article  Google Scholar 

  • Sauer, W. H. & M. R. Lipinski, 1990. Histological validation of morphological stages of sexual maturity in chokker squid Loligo vulgaris reynaudii D’Orb (Cephalopoda: Loliginidae). South African Journal of Marine Science 9: 189–200.

    Article  Google Scholar 

  • Silva, L., I. Sobrino & F. Ramos, 2002. Reproductive biology of the common octopus, Octopus vulgaris Cuvier, 1797 (Cephalopoda: Octopodidae) in the Gulf of Cádiz (SW Spain). Bulletin of Marine Science 71: 837–850.

    Google Scholar 

  • Tomkiewicz, J., L. Tybjerg & A. Jespersen, 2003. Micro- and macroscopic characteristics to stage gonadal maturation of female Baltic cod. Journal of Fish Biology 62: 253–275.

    Article  Google Scholar 

  • Vitale, F., H. Svedäg & M. Cardinale, 2006. Histological analysis invalidates macroscopically determined maturity ogives of the Kattegat cod (Gadus morhua) and suggests new proxies for estimating maturity status of individual fish. ICES Journal of Marine Science 63: 485–492.

    Article  Google Scholar 

  • Weibel, E. R., G. S. Kistler & W. F. Scherle, 1966. Practical stereological methods for morphometric cytology. The Journal of Cell Biology. 30: 23–38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West, G., 1990. Methods of assessing ovarian development in fishes: a review. Marine and Freshwater Research 41: 199–222.

    Article  Google Scholar 

  • Wood, S., 2006. Generalized Additive Models: An Introduction Using R. Chapman & Hall/CRC, Boca Raton.

    Google Scholar 

  • Zuur, A. F., E. N. Ieno, N. J. Walker, A. A. Saveliev & G. M. Smith, 2009. Mixed Effects Models and Extensions in Ecology with R. Springer, New York.

    Book  Google Scholar 

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Acknowledgements

We thank the “Asociación de Naseiros de Meira” for providing the majority of the octopus individuals, and Jose Manuel Antonio, Manuel. E. Garci, and María Teresa Fernández for their help in processing the samples. The Fisheries Group (CSIC) allowed us to use their image analyzer, and Alex Alonso in particular provided valuable support in the use of the stereological method and helpful suggestions during the manuscript preparation. This work was funded by the Comisión Interministerial de Ciencia y Tecnología (CICYT, Spain) (Project VEM 2003–2010). P. Sieiro was supported by a fellowship of Departamento de Postgrado y Especialización (CSIC), and J. Otero was supported by a “Junta para la Ampliación de Estudios” Fellowship (JAE-Doc programme 2011) from the CSIC and ESF. We also acknowledge the input of four anonymous reviewers that greatly improved the manuscript.

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  1. Centro Tecnológico del Mar, Fundación CETMAR, Eduardo Cabello s/n, 36208, Vigo, Spain

    Pilar Sieiro

  2. CSIC Instituto de Investigaciones Marinas, Eduardo Cabello 6, 36208, Vigo, Spain

    Jaime Otero & Ángel Guerra

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  1. Pilar Sieiro
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Correspondence to Pilar Sieiro.

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Sieiro, P., Otero, J. & Guerra, Á. Contrasting macroscopic maturity staging with histological characteristics of the gonads in female Octopus vulgaris . Hydrobiologia 730, 113–125 (2014). https://doi.org/10.1007/s10750-014-1826-4

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