The behavior and physiology of protandrous sex change in the Cinnamon anemonefish, Amphiprion melanopus

Abstract

Protandrous sex change was examined at the histological, endocrinological, and behavioral levels in the Cinnamon anemonefish, Amphiprion melanopus. The objectives were a detailed description of sex change in this species in nature and synthesis of changes at these three levels. The gonads of non-breeding juvenile fish develop initially along a female path. Males have an ovotestis with mature testicular tissue and immature ovarian tissue. Mature females possess no spermatogenic tissue. Sex change was stimulated in the field and gonadal changes were examined histologically. Five days after female removal, no gonadal changes were visible. Extensive spermatogenic maturation and early oogonial proliferation were seen by 10 days. Spermatogenic tissue was nearly completely replaced by previtellogenic oocytes by 20 days and the first indicators of vitellogenesis were observed at 45 days. Sex change was complete by 100 days. Plasma levels of five steroids were measured in males, females, and at five, 10, and 20 days into sex change. Females had higher levels of androstenedione, testosterone, and estradiol-17β than males and lower levels of l1-ketotestosterone. Cortisol levels were not different in males and females. Androgens decreased in the first ten days of sex change, then increased by 20 days. Estradiol-17β did not increase until 20 days into sex change, after critical early events of ovarian development. Estradiol-to-androgen ratios increased by five days. Cortisol increased over male levels during sex change, peaking at 20 days, then dropped to male levels in females. Females are the dominant and most aggressive members of social groups and display frequent aggression towards males. Aggression displayed by males increased significantly within one day following female removal, then decreased gradually. No convincing evidence for a role of androgens or estradiol in increased aggressive behavior during sex change was found either in overall patterns or within individuals. Cortisol appears linked to behavior, but whether as cause or effect is unclear. The pattern of sex-role reversal and androgens in A. melanopus is similar to that of polyandrous birds and supports recent theories of the role of steroid hormones in the control of behavior.