Seasonal changes of progesterone and testosterone concentrations throughout gonad maturation stages of the Mexican octopus, Octopus maya (Octopodidae: Octopus)

Abstract

Variations in progesterone (P₄) and testosterone (T) levels in the gonad of Octopus maya from Sisal in Yucatan State, Mexico, were investigated by radioimmunoassays and in relation to four gonad maturation stages (GMS) and to the reproductive cycle, as represented by two maturity indices (microscopic ‘MiMI’ and macroscopic ‘MaMI’). According to the GMS and the maturity indices, the reproductive season of O. maya from Yucatan occurred from February to June. In females, P₄ and T displayed the same pattern, with a tendency to increase at the same time, although on average, P₄ had seven-fold higher concentrations than T. In contrast, P₄ and T in male gonads displayed a different pattern, where T concentrations were relatively stable throughout all of the study months. In the female gonad P₄ was lowest (close to 0 pg g^–1) during both developing (GMS-I) and maturing (GMS-II) stages, and increased (189 ± 53 pg g^–1) approaching the mature stage (GMS-III) to a maximum value of 611 pg g^–1. Concentrations of T in the male gonad were lowest (106 ± 9 pg g^–1) during the maturing stage (GMS-II) and increased up to the mature stage (GMS-III), reaching a maximum of 440 pg g^–1. Pearson's correlation (r) between hormones and maturity indices showed strong relationships for females (around 0.4 and −0.7; p < 0.05), but there were negligible or weak relationships for males (0.2 and −0.1; p > 0.05). Hormone correlations in females were inverse with MaMI and direct with MiMI. Our major findings showed that gonadal P₄ levels were elevated during GMS-III and GMS-IV (i.e. periods of vitellogenic oocytes), where the characteristic aspect is an ovary with very high oocyte diameters, with the primary follicle cells deeply infolded in the ooplasm for yolk synthesis. These results suggested a synchrony between P₄ and the process of folliculogenesis, and in turn, vitellogenesis.

Keywords:

• radioimmunoassay
• sex steroids
• reproductive cycle
• maturity index
• reproductive season
• cephalopod

Acknowledgements

This research was partially funded by PAPIIT project number IN212012 and CONACYT CB: 2010–01/150810 to C Rosas. OH Avila-Poveda receives a CONACYT scholarship and a family grant and the results presented here are part of his PhD Dissertation. Thanks are due to the team Pulpo at Sisal for their professional gear handling, but we are especially grateful to Arturo George-Zamora and Felipe Briceño for their direct assistance in octopus sampling and laboratory work. The radioimmunoassay procedures were performed in the Radioimmunoassay laboratory of the Veterinary Medicine and Zootechnics School, Yucatan University (UADY-FMVZ), in accordance with the standard operating procedures given by the National Commission of Nuclear Safety and Safeguard of Mexico (CNSNS, acronym in Spanish, http://www.cnsns.gob.mx/). The critical appraisals of reviewers Anna Di Cosmo, Gianluca Polese and Kathrin Bolstad, and of one anonymous reviewer, are greatly appreciated. OH Avila-Poveda and LR Jimenez-Gutierrez were commissioned from CÁTEDRAS-CONACYT (project No. 2137/FACIMAR-UAS).

Disclosure statement

No potential conflict of interest was reported by the authors.

ORCID

Omar Hernando Avila-Poveda http://orcid.org/0000-0002-4411-0602

Rubén Cornelio Montes-Pérez http://orcid.org/0000-0003-4251-7342

Noussithé Koueta http://orcid.org/0000-0003-1791-2930

Francisco Benítez-Villalobos http://orcid.org/0000-0002-0951-7757

Jorge Saúl Ramírez-Pérez http://orcid.org/0000-0002-3994-424X

L.R. Jimenez-Gutierrez http://orcid.org/0000-0001-6805-4134

Carlos Rosas http://orcid.org/0000-0002-1301-7368