Reproduction and embryonic development of the red stingray Hemitrygon akajei from Ariake Bay, Japan

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. Gestation required 3 months with parturition during late July and early August. Uterine eggs without macroscopic embryos were observed during the first 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 fishing pressure. Producing high numbers of small young is a successful reproductive strategy for H. akajei that may be partly responsible for their resilience to fishing pressure and continued abundance in Ariake Bay. This study is the first to describe reproduction of H. akajei, an economically important top predator inhabiting coastal ecosystems throughout Asia.

Molecular mechanism of nutrient uptake in developing embryos of oviparous cloudy catshark (Scyliorhinus torazame)

“…Since the S . acanthias embryos are nourished by additional histotroph [ 2 , 46 – 48 ], yolk nutrients are likely essential only in the early developmental phase as embryonic nutrition subsequently transits to histotrophy in viviparous species.…”

“…A similar pattern in the yolk consumption during the embryonic period (slow in early period and fast in later period) is also observed in Japanese quail ( Coturnix japonica ) [ 61 ] and European plaice ( Pleuronectes platessa ) [ 62 ]. In other cartilaginous fishes, additional maternal nutrient supplies to the embryos are commonly found in viviparous species, and these nutrients are known to contribute the rapid embryonic growth in late developmental stages [ 2 , 48 , 63 ]. For example, embryos of great white shark ( Carcharodon carcharias ) ingest the maternal histotroph and digest nutrients by the gastrointestinal tract [ 2 ].…”

Sperm Lipid Composition in Early Diverged Fish Species: Internal vs. External Mode of Fertilization

“…A specific function of the sulfatides in mediating interactions between spermatozoa and components of the female genital duct was assumed for birds, which are known to store male gametes in female reproductive ducts [45]. Female stingrays are also assumed to store sperm for a prolonged period [46], like other cartilaginous fishes which can store sperm for a year and beyond [47,48]. In mammals, the sulfogalactosylglycerolipid, called seminolipid, is indispensable for spermatogenesis, sperm function, and fertilization (reviewed in [49]).…”

Factors affecting gestation periods in elasmobranch fishes

“…In our dataset, ringstreaked guitarfish Rhinobatos hynnicephalus and red stingray Hemitrygon akajei appear to exhibit embryonic diapause. During this diapause period, uterine eggs without macroscopic embryos are observed, and embryonic growth begins after this period ( Furumitsu et al, 2019 ; Kume et al, 2009 ). Hence, for these species, we estimated gestation periods as the length between the beginning and completion (i.e.…”

“…Elasmobranch is another taxonomic group that has many viviparous species. Their gestation periods vary among species from a few months to years ( Furumitsu et al, 2019 ; Hanchet, 1988 ). However, factors causing this variation are poorly understood.…”