Male reproductive cycle of hibernating Korean greater horseshoe bat,Rhinolophus ferrumequinum korai(Chiroptera: Rhinolophidae): annual cycle of the seminiferous epithelium and morphological changes of the testes

Abstract

Morphological changes of testes and the annual cycle of the seminiferous epithelium were observed by optical and transmission electron microscopy to determine the male reproductive cycle of the Korean greater horseshoe bat, Rhinolophus ferrumequinum korai. In this study, R. ferrumequinum korai showed a distinct reproductive cycle, unlike other hibernating bat species. The testicular reproductive cycle of R. ferrumequinum korai consists of three main stages. The first is the spermatogenesis stage (from April to September), including spermatocytogenesis (which appears from April to May) and spermiogenesis (from June to September). The activity of spermatogenesis was highest in August. The lumen of seminiferous tubules was open from mid-April to mid-October. It was closed from November to March of the following year. The second stage is the phagocytosis stage (from mid-October to mid-November), which is a purification process to prepare for new spermatogenesis the following year. This period is called the cleansing period. The third is the dormant stagethat is, a state of holding only spermatogonia and Sertoli cells. It is an adaptation strategy to store energy for long periods of hibernation. Compared to previous studies, spermatogenesis period preceded 1 month earlier. This suggests that temperature increase can impact reproductive development and spermatogenesis.

Three-Dimensional and Histological Observations on Male Genital Organs of Greater Horseshoe Bat, Rhinolophus ferrumequinum

“…In hibernating species with testes permanently located within the abdominal cavity (e.g., Rhinopoma hardwickei, Karim and Banerjee 1989;Rhinopoma kinneari, Anand Kumar 1965), spermatogenesis is more active in the winter, when hibernation takes place. On the contrary, in hibernating species with testes located outside the abdominal cavity (external type), spermatogenesis does not occur during hibernation periods (Lee 2018). Among Rhinolophus, the activation of spermatogenesis is reported to occur during the non-hibernating period in R. cornutus (August and October: Kurohmaru et al 2002) and R. capensis (October to November: Bernard 1985).…”

Female annual reproductive cycle ofRhinolophus ferrumequinum korai(Chiroptera: Rhinolophidae): morphological changes and prolonged sperm storage and sperm fate of the female reproductive tract according to month

“…Thus, the breeding cycle of a species should be explained on the basis of the breeding phenomenon in females and males. In other words, for the reproductive cycle of hibernating Korean greater horseshoe bats (R. ferrumequinum korai), mating is initiated August-September when spermatogenesis is active in males (Lee 2018a). During long-term hibernation after mating, immature sperm cells left in the male seminiferous tubule are completely removed by phagocytosis by Sertoli cells, which is called the cleansing period.…”

“…During long-term hibernation after mating, immature sperm cells left in the male seminiferous tubule are completely removed by phagocytosis by Sertoli cells, which is called the cleansing period. Such phagocytosis suggests the preparation period to produce new sperm from testicles (Lee 2018a). Additionally, sperm left Figure 6.…”

“…In particular, only the sperm reaching the caudal isthmus of the oviduct as the space for sperm storage engages in fertilization. For the annual female reproductive cycle in R. ferrumequinum korai, mating and ovulation as well as fertilization, implantation, delivery and the nurturing period occur approximately 1 month earlier than Rhinolophidae bats including most of the species belonging to Vespertilionidae (Table II), suggesting that such change and difference in reproductive cycle may contribute to photoperiod and temperature change as insisted by Lee (2018aLee ( , 2018b.…”

“…The male reproductive cycle of hibernating bats is classified as three types, "Pipistrellus pattern", "Myotis pattern" and "Miniopterus pattern", in consideration of sperm differentiation process and change in adnexal organs (Gustafson 1979). In particular, studies of serial events in testicles and sperm fate and loss in epididymis during the male reproductive cycle, conducted on temperate hibernating bats, are worthy of notice (Lee 2018a(Lee , 2018b.…”