Ichthyological Research https://doi.org/10.1007/s10228-019-00687-9 MONOGRAPH Reproduction and embryonic development of the red stingray Hemitrygon akajei from Ariake Bay, Japan Keisuke Furumitsu1 · Jennifer T. Wyfels2,3 · Atsuko Yamaguchi1 Received: 6 September 2018 / Revised: 18 December 2018 / Accepted: 24 February 2019 © The Author(s) 2019 Abstract The reproductive system of the red stingray Hemitrygon akajei was described from 1,418 specimens, 682 males and 736 females, sampled year-round (2003–2014) from Ariake Bay to provide reproductive life history information for conservation and management of the species. Females reach sexual maturity at a larger size than males with the size at 50% sexual maturity 522.2 mm disc width (DW) and 321.5 mm DW, respectively. Male stingrays had semen in the seminal vesicles year-round. Dental sexual dimorphism was aseasonal. The mating period is protracted, spanning 7 consecutive months October–April but ovulation occurred during May. This suggests female sperm storage, which has not been described for dasyatid stingrays. Females have a single functional ovary and uterus (left) and reproduce via aplacental viviparity with lipid histotrophy. Gesta- tion required 3 months with parturition during late July and early August. Uterine eggs without macroscopic embryos were observed during the frst half of gestation suggesting a short period of arrested development or diapause. Developmental cohorts based on morphological features were described for embryos and can be used to characterize embryo growth and development for other stingray species. Observations of foetal mortality (1.25%) and morphologically abnormal embryos (0.72%) were uncommon. Pregnancy rate was 90% and reproduction was annual and synchronous. Hemitrygon akajei fecundity ranged from 7 to 25 and increased with female size. Although H. akajei is a medium-sized dasyatid ray, it has the highest fecundity reported for any batoid species. Elasmobranchs life histories usually are associated with a low degree of productivity that results in rapid population decline with increased fshing pressure. Producing high numbers of small young is a successful reproductive strategy for H. akajei that may be partly responsible for their resilience to fshing pressure and continued abundance in Ariake Bay. This study is the frst to describe reproduction of H. akajei, an economically important top predator inhabiting coastal ecosystems throughout Asia. Keywords Fecundity · Spermatogenesis · Sperm storage · Diapause · Dasyatidae Introduction Hemitrygon akajei is a whiptail stingray (Chondrichthyes: Dasyatidae) that inhabits sandy bottoms of temperate to Electronic supplementary material The online version of this article (https ://doi.org/10.1007/s1022 8-019-00687 -9) contains tropical seas of the Northwest Pacifc (Yamaguchi et al. supplementary material, which is available to authorized users. 2013). Hemitrygon akajei is endemic to Asia, known from Japan, Korea, Taiwan, China, Thailand (east coast), Malay- * Atsuko Yamaguchi sia and Indonesia (Yano et al. 2005; Yamaguchi et al. 2013) [email protected] and also from the Russian Federation, albeit with less fre- 1 Graduate School of Fisheries and Environmental Sciences, quency (Yamaguchi et al. 2013). In Japan, H. akajei is a Nagasaki University, 1-14 Bunkyo, Nagasaki 852-8521, common species found in coastal areas including brack- Japan ish waters from Hokkaido to the Ogasawara Islands and 2 Center for Bioinformatics and Computational Biology, Okinawa (Amaoka et al. 1989; Randall et al. 1997; Shino- Computer and Information Sciences, University of Delaware, hara et al. 2005). Newark, DE 19711, USA Ariake Bay, located in Kyushu, is one of the most produc- 3 South-East Zoo Alliance for Reproduction & Conservation, tive bays in Japan (Takita and Yamaguchi 2009). Ariake Bay Yulee, FL 32097, USA Vol.:(0123456789)1 3 K. Furumitsu et al. has high species diversity and a large resident population of fecundity ranges from 1 for Hypanus marianae (Yokota and elasmobranchs including fve described and one undescribed Lessa 2007) and Megatrygon microps (Nair and Soundara- Dasyatidae species (Furumitsu and Yamaguchi 2010). Elas- rajan 1976; Pierce et al. 2008) to 13 for H. akajei (Hagiwara mobranchs are non-target species caught by bottom trawlers 1993) and Pteroplatytrygon violacea (Wilson and Beckett targeting shrimps in summer and fshes in general during 1970). Dasyatid stingrays range from 30 cm (pale-edge winter and comprise as much as 70–80% of the total catch sharpnose ray Telatrygon zugei) to more than 2 m (roughtail (by mass) (Yamaguchi 2005). Hemitrygon akajei is the most stingray Bathytoshia centroura) in disc width (DW) (Last common dasyatid caught by gill net (year-round), bottom et al. 2016). Fecundity increases with female size for select trawl (May–August and November–February) and longline species, but this relationship cannot be generalized for all fsheries (year-round) (Yamaguchi 2009). dasyatids. According to the IUCN Red List, landings of H. akajei Hemitrygon akajei is classifed as “Near Threatened” are declining (Huveneers and Ishihara 2016). In 1972, the (NT) by the IUCN Red List (Huveneers and Ishihara 2016). total catch of stingrays in Ariake Bay was 42 tons. Stingray To accurately assess the current population status, impacts landings increased to 310 tons in 1988, and subsequently of fshing pressure and biological niche of H. akajei in Ari- declined to 113 tons in 2006, but no data concerning fshing ake Bay’s ecosystem, information about the life history and efort during the same time frame is available for compari- especially reproductive habits of H. akajei is needed. Repro- son (Kyushu Regional Agricultural Administration Ofce ductive periodicity, seasonality and variables such as size 1973–2007). A predator control program was implemented at maturity and fecundity are helpful to manage stocks and in 2001 to protect shellfsh in Ariake Bay, and H. akajei was maintain a sustainable fshery. Given the lack of life his- taken as part of that program; however, catch data are not tory information for this species throughout its range and available to determine the impact of the predator control its value as a fsheries resource, the aim of this study was program on H. akajei or other species (Yamaguchi 2009). to characterize the reproductive biology of H. akajei from Current landing records for H. akajei in Ariake Bay are not Ariake Bay including embryonic development and foetal publicly available, preventing an assessment of changes in mortality rate. population size, distribution and trends over time. Despite a commercial fshery and predator control pro- gram that target H. akajei, there are few biological stud- Materials and methods ies of this species throughout its range and, consequently, little is known about its biology. The feeding habits of H. Study location and survey techniques. Ariake Bay is located akajei from Tokyo Bay have been characterized (Taniuchi in western Kyushu and has a gross area of 1,700 km2 and Shimizu 1993). Dental sexual dimorphism, where males (Fig. 1). The bay has extremely specifc local environmental develop pointed cuspidate dentition to bite and hold females features including large tidal ranges (maximum 6 metres), during copulation, is widespread among batoids and has fast currents and expansive tidal fats. The tidal fat area for been described for H. akajei from Tokyo Bay (Bigelow and this bay is the greatest in all of Japan with a gross area of Schroeder 1953; Taniuchi and Shimizu 1993; Nordell 1994; 180–190 km2. The northern part of the bay is shallow with Kajiura and Tricas 1996). Temporal changes in tooth mor- a depth less than 20 m, while the southern part of the bay phology associated with the mating season that have been is relatively deep. The mouth of the bay is the deepest area observed for some dasyatid stingrays have not been investi- in the southern bay, almost 200 m deep and very narrow, gated for H. akajei (Taniuchi and Shimizu 1993; Kajiura and forming a bottleneck barrier or pseudo-closed bay. Mixing Tricas 1996). Observations of mating behaviour and parturi- with oceanic waters occurs at the mouth of the bay. Stingray tion for H. akajei were described from stingrays observed in specimens were sampled monthly April 2003–April 2014 aquaria (Hagiwara 1993). from the catch of commercial fshing vessels operating in There has been no study of the reproductive biology of H. regional fsheries in Ariake Bay. Set nets were used in area akajei throughout its range, but some reproductive traits are A (3–8 m deep, an estuary), gill nets and set nets in area B common among dasyatids. Dasyatid stingrays have a single (8–20 m deep), bottom trawlers in area C (35–65 m deep) functional left ovary and uterus and reproduce via aplacen- and longlines in all three areas (3–200 m deep) (Fig. 1). tal viviparity with lipid histotrophy (Capapé 1976; Snelson Morphometrics and reproductive data. Disc width (DW, et al. 1988; Ribeiro et al. 2006; Veras et al. 2014). Mating is nearest 0.5 mm), body mass (BM, nearest 0.001 g for followed immediately by ovulation and fertilization with no embryos or 1 g for feld specimens) and sex were recorded evidence for female sperm storage. Gestation may include for each ray. The total number and number of mature males embryonic diapause, a temporary period of suspended or and females in the northern (A and B) and southern (C) arrested embryonic development (Snelson et al. 1989; Mor- areas were subjected to a Chi squared (χ2) test to deter- ris 1999; Wyfels 2009; Waltrick et al. 2012). Maximum mine if they difered from parity. For females, presence or 1 3 Hemitrygon akajei reproduction and embryonic development Fig. 1 Location and sampling area for Hemitrygon akajei for fsh examined from 2003 to 2014. Three regions of Ariake Bay were sampled, the estuary area (A), the northern region (B) and the southern region (C) absence of semen in the cloaca and cervix was noted and Parameters were derived using the statistical software uterus mass (UM, nearest 0.1 g) was measured.