Microscopic organization of the sperm storage tubules in the oviducal gland of the female gummy shark (Mustelus antarcticus), with observations on sperm distribution and storage

Abstract

Oviducal gland morphology, the microscopic organization of the terminal zone, and sperm storage were described in the female gummy shark (Mustelus antarcticus). Mustelus antarcticus is a nonplacental viviparous hound shark, which displays minimal histotrophy during embryonic development. The animals examined represented all stages of maturity and gestation. The oviducal gland was found to have the same fundamental zonation as in most chondrichthyans. Using recent terminology, the oviducal gland of chondrichthyans has an anterior club zone, followed by a papillary zone, both of which produce jelly that surrounds the egg, a baffle zone that elaborates the tertiary egg envelope and a terminal zone, where sperm storage occurs. Each zone is composed of simple tubular glands that connect to transverse grooves, which extend the full width of the gland. The exception is the terminal zone, which does not have transverse grooves but consists of individual tubules. The microscopic organization and histochemical nature of the zones display similar patterns to those of other chondrichthyan genera. Tubules of the terminal zone contain four types of cell: ciliated cells, alcian blue-positive secretory cells, periodic acid-Schiff and alcian blue-negative secretory cells, and secretory columnar cells. These tubules end in recesses, the sperm storage tubules, which extend beyond the periphery of the baffle zone. Sperm were stored in the sperm storage tubules of all maturing and mature animals examined. Of note is the observation of stored sperm in an animal 1 year prior to first ovulation. Sperm were also observed throughout the uterine sphincter, body of the uterus, isthmus, and oviduct of maturing and mature animals, and in the uterine sphincter of an immature animal. These sperm represent immediately postcopulation aggregations of sperm and sperm in the process of migrating to the site of storage or to the site of fertilization.

Morphological analysis of the oviduct, oviducal gland and isthmus of the blue shark Prionace glauca (Linnaeus, 1758) (Elasmobranchii: Carcharhiniformes)

“…The oviduct and isthmus observed macro and microscopically were very similar to those present in Mustelus antarcticus (Storrie et al, 2008) and Iago omanensis (Fishelson & Baranes, 1998;Hamlett et al, 2002), both placental viviparous species, like P. glauca. According to Pratt (1979), the oviduct in P. glauca expands to form the oviducal gland and then returns to its original diameter of approximately 10 mm; this area is called the isthmus.…”

“…The club and papillary zones have the same morphology as observed in other species, especially in Mustelus antarcticus (Storrie et al, 2008), with only some differences in the shape and number of glandular tubules. Earlier descriptions generally refer to the club zone as the albumen zone and the papillary zone as the mucous zone (Hamlett et al, 1998;Hamlett & Koob, 1999).…”

“…The oviducal gland of P. glauca has the same morphological characteristics observed in other elasmobranchs (Hamlett et al, 1998(Hamlett et al, , 2002Storrie et al, 2008;Moura et al, 2011). However, Mattews (1950) studied the reproductive system of Cetorhinus maximus, a shark species of the family Laminidae with aplacental viviparous reproduction of type Oophagia, and described the oviducal gland as a structure different from that of other elasmobranchs: apparently uniform, without clear divisions and without any sign of secretion of shell material.…”

“…Twenty of these 38 females were classified as in pre-ovulation, three were in post-ovulation, two were sub-adult, and 13 were pregnant. Storrie et al (2008) also reported the presence of sperm in M. antarcticus both in pregnant, mature non-pregnant, postpartum and immature females throughout the year.…”

“…Hamlett et al (1998) observed that despite the variations between species regarding the different reproductive strategies, the same basic functional design is present in the species studied by them. Four zones are distinguished in most of the studied species: an anterior club zone, followed by a papillary zone that produces mucus that surrounds the fertilized ovum in the early stages of embryogenesis, a baffle zone that forms the tertiary envelope of the egg, and a terminal zone where the sperm is stored (Hamlett et al, 1998;Hamlett & Koob, 1999;Hamlett et al, 2005;Storrie et al, 2008).…”