The flexible survival strategy of the East Asian species Naru eagle ray under harsh environments was revealed by Nagasaki University and others

Based on a 19 year long-term field study the research group of Professor Atsuko Yamaguchi and Researcher Keisuke Furumitsu of the Graduate School of Fisheries and Environmental Sciences, Nagasaki University, and Dr. Jennifer Wyffels of the University of Delaware have comprehensively clarified the reproductive system and ecology of a rare species of eagle ray (family Mylobatidae) found in East Asia. In addition, for the first time, they clarified the phenomenon of embryonic diapause, which is still largely unknown in fish, including those of the order Elasmobranchii (sharks and rays). They also clarified the ecological significance of embryonic diapause and the rapid fetal development process after dormancy.

It was noted that Naru eagle rays increased in the Ariake Sea along with temperature increases due to global warming. Since they preferentially feed on shellfish, the species is suspected to cause predation damage to Japanese littleneck clams (Lajonkairia lajonkairii) and pen shells (Atrina pectinata). Rays have declined as a result of continuous public predator control programs over the last 20 years, and there are concerns on the impact of the process on the ecosystem. Initially, there was no scientific knowledge about these rays, and in the process of ecological research by Professor Yamaguchi, it became clear that the Naru eagle ray was actually a new species, and a new scientific name (Aetobatus narutobiei) was assigned in 2013. Elasmobranchii breeding patterns include both oviparous and viviparous births, and particularly, it was difficult to study the early development of embryonic rays because many of their developmental processes were shrouded in mystery. However, Professor Yamaguchi's group, for the first time, clarified the details of the embryonic development process of coastal stingrays in 2019.

In this study, they succeeded in grasping the difficult to study development process of the Naru eagle ray embryo in more detail. It is the first time in the world that they have been able to record in detail how a baby ray is formed in the womb after it develops from a fertilized egg.

The Naru eagle ray reproduces via matrotrophic histotrophy, where an embryo is fertilized immediately after copulation in the female's body and growth pauses shortly after embryonic development begins in the uterus. The embryo then lies dormant for approximately 9.5 months out of the 12 month gestation period. Embryos that awaken from dormancy undergo remarkable growth in only 2.5 months and are born. The developmental process of the embryo in the uterus was described in detail and classified into 11 stages, and the embryo at each stage were successfully photographed.

Early development depends on the vitellus (the yolk); however, the morphology of the ray is almost complete by the time the external yolk sac is absorbed. The embryo takes in the tissue nutrients (called uterine milk) secreted into the uterus during the latter half of pregnancy and grows even larger. The embryo reaches a weight that is 346 times that of the newly fertilized egg. It is said to be the greatest growth rate among embryonic ray species. The average number of offspring at one time is three, which is an extremely low fertility among embryonic rays with two functional uteri on the left and right.

After giving birth and mating, the Naru eagle ray stores energy for wintering and leaves the shallow waters of the Ariake Sea to overwinter in the open sea from late autumn to late spring when the water temperature drops significantly due to the influence of land areas. Long-lasting embryonic diapause of the Naru eagle ray allows the females to minimize the energy demands required for reproduction during migration to the open sea and overwintering. They copulate before overwintering when the risk of mortality is increased for males with high natural mortality. Embryonic diapause also allows all reproductive events (gonadal development, pregnancy, childbirth, and copulation) to be concentrated in summer, causing a delay in the birth of newborns until the summer, which is the optimal period for their survival. Embryonic diapause is a beneficial survival strategy not only for newborns but also for adult fish, and it may lead to successful reproduction and enhanced survival via flexible adaptation in harsh environments for the Naru eagle ray. It is difficult to quickly restore the population declines that the Naru eagle rays have experienced due to the continuous strong capture pressure in their breeding ground, even from the viewpoint of their breeding characteristics. In the future, it will be necessary to conserve and manage rays based on scientific evidence. This comprehensive understanding of reproductive and survival strategies will contribute to the field of biology, evolution, and ecology as a first step toward clarifying the unknown mode of reproduction of fish.

■ Embryonic diapause, a reproductive strategy that has evolved to maximize survival and reproductive success rates, is a regulatory phenomenon for giving birth at an optimal time by stopping embryo development and prolonging gestation.