Effects of the dominance hierarchy on social interactions, cortisol level, HPG-axis activities and reproductive success in the golden cuttlefish Sepia esculenta

Abstract

Dominance hierarchies are ubiquitous among group-living animals and markedly affect growth performance, metabolism, agonistic interactions, and stress-related physiology in vertebrates. However, few studies have investigated the effects of dominance hierarchies on the hypothalamic-pituitary-gonadal (HPG) axis and reproduction, especially in cephalopods. In this study, we employed an economically important cephalopod, the golden cuttlefish Sepia esculenta, as the target animal. Adopting the classical paired design, we first identified the formation of a dominance hierarchy and then investigated its effects on social interactions, cortisol level, HPG-axis activities (as indicated by the concentrations of gonadotrophin-releasing hormone (GnRH) and estradiol and the mRNA abundances of gnrh and estrogen receptor (er) genes), and reproductive success (determined by parentage analysis using polymorphic microsatellite loci) during the reproductive period. In general, dominant individuals presented significantly higher frequencies of aggressive behaviors (categorized as attack, chase, displace and threaten behaviors) and reproductive behaviors (designated mating events for males and spawning events for females), lower cortisol concentrations, higher HPG-axis activities, and higher reproductive success than subordinate individuals (all P < 0.05). Strong correlations between the frequencies of reproductive behaviors and reproductive success and among cortisol levels, HPG-axis activities and reproductive success were observed. However, no significant differences between dominant and subordinate individuals in body weight, dorsal mantle length or dorsal mantle width were detected. These results clearly show that dominance hierarchies occur in golden cuttlefish and provide the first evidence that such hierarchies significantly affect stress physiology, HPG-axis activities, and reproductive success in cephalopods. In the aquaculture and artificial reproduction of golden cuttlefish, we suggest that measures be adopted to decrease or eliminate harmful agonistic interactions and the subsequent physiological stress caused by dominance hierarchies to increase the reproductive efficiency.