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Ultrastructure of the Reproductive System of the Black Swamp Snake (Seminatrix Pygaea). II. Annual Oviducal Cycle

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Ultrastructure of the Reproductive System of the Black Swamp Snake (Seminatrix Pygaea). II. Annual Oviducal Cycle JOURNAL OF MORPHOLOGY 245:146–160 (2000) Ultrastructure of the Reproductive System of the Black Swamp Snake (Seminatrix pygaea). II. Annual Oviducal Cycle David M. Sever,1* Travis J. Ryan,2,3 Terasa Morris,1 Deborah Patton,1 and Shannon Swafford1 1Department of Biology, Saint Mary’s College, Notre Dame, Indiana 2Division of Biological Sciences, University of Missouri, Columbia, Missouri 3Savannah River Ecology Laboratory, Aiken, South Carolina ABSTRACT This article is the first ultrastructural nar, and cells with elongate cilia alternate with secretory study on the annual oviducal cycle in a snake. The ultra- cells. The secretory product of the infundibulum consists structure of the oviduct was studied in 21 females of the largely of lipids, whereas a glycoprotein predominates in viviparous natricine snake Seminatrix pygaea. Specimens the vagina; however, both products are found in these were collected and sacrificed in March, May, June, July, regions and elsewhere in the oviduct. In the SST area and and October from one locale in South Carolina during the anterior vagina, tubular glands are compound as well 1998–1999. The sample included individuals: 1) in an as simple. The epithelium of the SST is most active after inactive reproductive condition, 2) mated but prior to ovu- mating, and glycoprotein vacuoles and lipid droplets are lation, and 3) from early and late periods of gravidity. The equally abundant. When present, sperm form tangled oviduct possesses four distinct regions from cranial to masses in the oviducal lumen and glands of the SST area. caudal: the anterior infundibulum, the posterior infundib- The glands of the uterus are always simple. During sperm ulum containing sperm storage tubules (SSTs), the migration, a carrier matrix composed of sloughed epithe- uterus, and the vagina. The epithelium is simple through- lial cells, a glycoprotein colloid, lipids, and membranous out the oviduct and invaginations of the lining form tubu- structures surround sperm in the posterior uterus. During lar glands in all regions except the anterior infundibulum gravidity, tubular glands, cilia, and secretory products and the posterior vagina. The tubular glands are not al- diminish with increasing development of the fetus, and veolar, as reported in some other snakes, and simply rep- numerous capillaries abut the basal lamina of the atten- resent a continuation of the oviducal lining with no addi- uated epithelial lining of the uterus. J. Morphol. 245: tional specializations. The anterior infundibulum and 146–160, 2000. © 2000 Wiley-Liss, Inc. vagina show the least amount of variation in relation to season or reproductive condition. In these regions, the KEY WORDS: Reptilia; Serpentes; Seminatrix pygaea; epithelium is irregular, varying from squamous to colum- ultrastructure; oviduct Numerous articles exist on the oviducal anatomy gions throughout the reproductive cycle. Other con- of squamate reptiles (see reviews by Fox, 1977; tributions in this series will deal with ultrastructure Blackburn, 1998), but relatively few of these studies of the male reproductive system. have specifically addressed the ultrastructure of the Seminatrix pygaea is a small (20–40 cm snout– oviduct in squamates (Hoffman, 1970; Hoffman and vent length as adults), highly aquatic snake limited Wimsatt, 1972; Bou-Resli et al., 1981; Perkins and to the southern Atlantic coastal plain (Dorcas et al., Palmer, 1996; Girling et al., 1997, 1998). As a part of 1998). The species ovulates large, yolky eggs and is a comprehensive study of reproduction in the Black viviparous by lecithotrophy, i.e., most if not all nu- Swamp Snake (Seminatrix pygaea Cope), we have trients for fetal development are supplied via the undertaken an analysis of various ultrastructural yolk of the ovulated ovum (Stewart, 1992; Stewart et features of the oviduct of this viviparous snake. Part al., 1990). The population of the species that we I dealt with transport of sperm and sperm storage in sampled is the largest known for the species (Gib- the oviduct (Sever and Ryan, 1999). Ultrastructural details of a carrier matrix in the uterus and sperm storage tubules (SSTs) in the posterior infundibu- lum (uterine tube) were described (Sever and Ryan, Contract grant sponsor: U.S. Department of Energy to the Univer- 1999). Another part will deal with the cytological sity of Georgia Research Foundation; Contract grant number: DE- relationships between the uterine lining and the FCO9-96SR18546. embryonic membranes. In this article, we report *Correspondence to: David M. Sever, Department of Biology, Saint more general aspects of oviducal cytology, with an Mary’s College, Notre Dame, IN 46556. emphasis on the ultrastructure of the various re- E-mail: [email protected] © 2000 WILEY-LISS, INC. REPRODUCTIVE SYSTEM OF SEMINATRIX PYGAEA 147 TABLE 1. Specimens used in this study Date Follicles/Eggs sacrificed SVL (cm) Location N Range Mean (mm) SE 31 March 22.2 Ovaries 5R 5L 2.0–2.9 2.5 0.09 25.3 Ovaries 5R 5L 1.9–2.8 2.5 0.11 29.3 Ovaries 8R 11L 1.8–3.5 2.6 0.12 31.0 Ovaries 9R 8L 2.2–3.6 3.0 0.10 32.9 Ovaries 11R 11L 2.4–3.9 3.2 0.10 14 May 98 23.7 Ovaries 6R 6L 1.8–3.1 2.4 0.11 28.0 Ovaries 5R 3L 5.0–7.2 5.8 0.35 32.0 Ovaries 10R 7L 1.8–3.5 2.7 0.12 33.0 Ovaries 5R 4L 7.0–11.2 9.6 0.47 9 June 26.0 Uteri 3R 2L 7.4–11.2 9.2 0.78 29.0 Uteri 3R 1L 17.5–18.2 17.9 0.14 30.2 Uteri 5R 3L 13.0–15.3 13.9 0.31 35.5 Ovaries 5R 5L 2.0–3.6 2.7 0.14 30 July 29.0 Ovaries 7R 3L 1.7–2.2 2.0 0.05 Uteri 2R 2L* 27.5 Ovaries 6R 5L 1.8–2.6 2.2 0.08 27.5 Ovaries 6R 4L 1.8–2.3 2.0 0.06 24.0 Ovaries 5R 3L 1.4–2.0 1.7 0.06 8 October 26.0 Ovaries 7R 7L 2.0–3.8 2.9 0.14 29.1 Ovaries 7R 9L 1.5–3.0 2.2 0.11 30.1 Ovaries 13R 10L 1.2–3.3 2.4 0.12 33.0 Ovaries 11R 7L 1.5–2.6 2.1 0.08 37.4 Ovaries 14R 11L 1.8–3.6 2.7 0.10 *Four fully formed fetuses, two of which were preserved in situ; other two measured 95 mm and 97 mm SVL. bons and Semlitsch, 1991), and other aspects of the preserved in 10% neutral buffered formalin (NBF) female reproductive cycle of this population were and housed in the research collections at Saint described by Seigel et al. (1995). They reported rapid Mary’s College. follicle growth in spring after hibernation, ovulation After death, the cloaca and both oviducts were in early June, and parturition in early August (Sei- removed in their entirety and fixed in a 1:1 solution gel et al., 1995). Because the reproductive cycle has of 2.5% glutaraldehyde in Millonig’s phosphate been well-studied (and continues to be monitored) buffer at pH 7.4 and 3.7% formaldehyde buffered to and seasonal samples are readily obtainable, fe- pH 7.2 with monobasic and dibasic phosphate. Fol- males from this population of S. pygaea are ideal for lowing the criteria of Blackburn (1998), three basic the first comprehensive studies on the oviducal ul- divisions of the oviduct could be recognized grossly: trastructure of a viviparous snake. infundibulum (with a posterior region of sperm stor- age tubules, SSTs), uterus, and vagina. The poste- rior infundibulum where SSTs are found has been MATERIALS AND METHODS referred to as the uterine tube by some authors (e.g., Specimens of Seminatrix pygaea were collected at Perkins and Palmer, 1996). Ellenton Bay, located on the Department of Energy’s For transmission electron microscopy (TEM), sec- Savannah River Site in Aiken County, South Caro- tions of the oviduct 2 mm in length were removed lina. Ellenton Bay is a shallow (2 m maximum from each division of the right oviduct. Tissue was depth), 10 ha freshwater “Carolina bay” that is rel- taken from the anterior portion of the infundibulum atively permanent (Gibbons and Semlitsch, 1991). as well as the SST area. From the uterine area, Collections were made during four periods in 1998 tissue was taken from both the anterior and poste- (10 May, 7 June, 22–24 July, and 29 September–2 rior ends of the uterus in nongravid snakes, whereas October), and one period in 1999 (17—22 March). in gravid snakes tissue was taken from the uterine Specimens were sacrificed within a week of capture lining surrounding an embryo (incubation chamber) (Table 1). Specimens were collected in unbaited min- and from the interembryonic area between eggs. now traps and from under coverboards alongside the After initial fixation, tissues were rinsed in water, bay. The reptiles of Ellenton Bay are the subjects of postfixed in 2% osmium tetroxide, and dehydrated long-term monitoring studies. In order to minimize through a graded series of alcohol. the ecological effects caused by removal of snakes, Tissues were subsequently cleared in propylene we limited each sample to a maximum of five adult oxide and immersed in increasing concentrations of female snakes. Specimens were killed by a lethal an epoxy resin (EmBed 812, Electron Microscopy injection (3–5 ml) of Nembutal (Abbott Laboratories, Sciences, Fort Washington, PA) in absolute ethanol North Chicago, IL). Carcasses of all specimens were before polymerization in pure resin for 36 h at 60°C.
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