Sexual maturation and embryonic development in octopus: use of energy and antioxidant defence mechanisms usingOctopus mimusas a model

Abstract

Sexual maturation and reproduction influence the status of a number of physiological processes and consequently the ecology and behaviour of cephalopods. Using Octopus mimus as model species, the present study examined the changes in biochemical composition that take place during gonadal maturation of octopus females and its consequences in embryo and hatchlings characteristics, including energetic metabolites, digestive enzymes and antioxidant defence mechanisms. A total of 32 Octopus mimus adult females were sampled during ovarian maturation; biochemical composition (metabolites and digestive enzymes) of digestive gland (DG) and ovaries (only metabolites) were followed during physiological and functional maturation. Levels of protein (Prot), triacyl glycerol (TG), cholesterol (Chol), glucose (Glu) and glycogen (Gly) were evaluated. The activity of alkaline and acidic enzymes also was measured in DG. Simultaneously, groups of eggs coming from mature females were sampled along development, and metabolites (Prot, TG, Glu, Gly, TG, Chol), digestive enzymes activity (Lipases, alkaline and acidic), antioxidant defence mechanisms and radical oxygen species (ROS) were evaluated. This study shows that ovarium is a site for reserve of some nutrients for reproduction. Presumably, TG where stored at the beginning of the maturation processes followed by Chol, both at the same time were energetically supported by Glu, derived from Gly following gluconeogenic pathways. Nutrients and enzymes (metabolic, digestive and REDOX system) where maintained without significant changes and in a low activity during organogenesis. Our findings suggest that activity was not energetically costly; in contrast, during the embryo growth there was mobilization of nutrients and activation of the metabolic and digestive enzymes. Increments in consumption of yolk and glycogen, and reduction in molecules associated with oxidative stress allowed paralarvae to hatch with the antioxidant defence mechanisms ready to support ROS production.

How hard is Octopus maya embryo’s life?

“…In the present study a considerable increase of SOD, CAT and GsT was observed from the activation stage onwards, when the circulatory system is activated in stages XIV -XVI. That pattern was also observed in O. mimus embryos 39 indicating that antioxidant defense mechanisms are also activated as a response against the embryo ROS production, resulting as the energy production increment to support the embryo growth phase. Catalase is one of the ROS detoxifying enzymes that can be found in the early embryonic development stages, observed that its activity remains practically stable until hatching in several species [40][41][42] .…”

“…6). In general, in O. maya -as in other cephalopod speciesbiochemical and molecular processes are highly dynamic during embryonic development 30,38,39 .…”

“…In O. maya embryos, vascularization and antioxidant response coincided during the organogenesis stage, indicating that the circulatory system and ROS neutralization are coordinated. It is essential to consider that femaleinherited ROS could alter these processes, mainly when the parents are exposed to thermal stress 39 . In addition, while the circulatory system remains incomplete, O 2 supply to developing embryonic cells could be diffusion limited, which could lead to a lack of energy.…”