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SHORT COMMUNICATIONS: Localization of Oviductal Sperm- Storage Tubules in the American Kestrel (Falco Sparverius)

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SHORT COMMUNICATIONS: Localization of Oviductal Sperm- Storage Tubules in the American Kestrel (Falco Sparverius) University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln U.S. Department of Agriculture: Agricultural Publications from USDA-ARS / UNL Faculty Research Service, Lincoln, Nebraska 1987 SHORT COMMUNICATIONS: Localization of Oviductal Sperm- storage Tubules in the American Kestrel (Falco sparverius) Murray R. Bakst United States Department of Agriculture David M. Bird McGill University Follow this and additional works at: https://digitalcommons.unl.edu/usdaarsfacpub Part of the Agricultural Science Commons Bakst, Murray R. and Bird, David M., "SHORT COMMUNICATIONS: Localization of Oviductal Sperm-storage Tubules in the American Kestrel (Falco sparverius)" (1987). Publications from USDA-ARS / UNL Faculty. 619. https://digitalcommons.unl.edu/usdaarsfacpub/619 This Article is brought to you for free and open access by the U.S. Department of Agriculture: Agricultural Research Service, Lincoln, Nebraska at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Publications from USDA-ARS / UNL Faculty by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. The Auk, Vol. 104, No. 2 (Apr., 1987), pp. 321-324 SHORT COMMUNICATIONS Localization of Oviductal Sperm-storageTubules in the American Kestrel (Falco sparverius) MuRRAY R. BAKST' AND DAVID M. BIRD2 'Avian Physiology Laboratory,Agricultural Research Service, U.S. Department of Agriculture, Beltsville, Maryland 20705 USA, and 2MacdonaldRaptor Research Centre, Macdonald Campus of McGill University, Ste. Anne de Bellevue, Quebec H9X 1CO,Canada Sperm-storage tubules (SST) are discrete tubular moved with iris scissors, immersed in a plastic dish invaginations of the bird's oviduct epithelium locat- containing PBS, and examined under a Zeiss SR Ste- ed in the anterior end of the vaginal folds, a region reophotomicroscope using transillumination (the generally referred to as the uterovaginal junction light beam is parallel to the base of the microscope (UVJ). [We prefer to refer to the UVJ sperm-storage and directed to the isolated fold). With unfixed sites collectively as the SST (originally used by Mero chicken or turkey specimens, long pieces of tissue and Ogasawara 1970) because SST accurately de- (3-4 cm) can be isolated (M. Bakst unpubl. data). In scribes their function and structure.] Of the 27 rec- fresh, unfixed tissue the SST are easily visualized and ognized orders of birds, SST have been identified can be manipulated to facilitate making squash prep- histologically only in selected species of Charadri- arations. However, fixation renders the mucosa sur- iformes and Procellariformes (Hatch 1983), Galli- rounding the SST more opaque and considerably less formes (Fujii and Tamura 1963), Anseriformes (Pal pliable. Pieces of NBF-fixed American Kestrel UVJ 1977), and Passeriformes (Bray et al. 1975). Whether mucosa less than 1 mm long were examined as above SST are structures common to all birds, as suggested to visualize individual SST. Once the precise location by Gilbert (1979) and Hatch (1983), remains to be of the SST was determined, the oviductal segment investigated. containing the SST was excised and processed for The presence of SST has not been demonstrated light microscopy. Paraffin sections (5-6 Am thick) were histologically in the Falconiformes. The high fre- stained with periodic-acid Schiff (PAS) with and quency of copulations in the course of laying one without a hematoxylin (H) counterstain. clutch of eggs prompted Corten (1973) to suggest that Morphology of the UVJ and SST.-Macroscopic in- SST do not exist in the Northern Goshawk (Accipiter spection of the American Kestrel uterus and vagina gentilis). Bird and Buckland (1976) observed the mean revealed longitudinally oriented folds that are rela- duration of fertility following artificial insemination tively wide at the uterus, narrow abruptly at the UVJ, of the American Kestrel (Falco sparverius) to be 8.1 and then continue through the vagina (Fig. 1). Light days (range = 4-12 days). They suggested that SST microscopy revealed an oviductal luminal surface ep- were present in the oviduct. We present evidence ithelium that consisted of alternating columnar cil- that SST exist at the UVJ of the American Kestrel. In iated and nonciliated secretory cells, the latter stained addition, a technique for the precise localization and considerably more intensely with PAS/H than the isolation of oviductal mucosa containing SST is de- former. Tubular glands (Fig. 2) underlie the surface scribed. epithelium in the uterus, and probably contribute to Localization and isolation of SST.-Three females its more voluminous folds (compared with the va- maintained as previously described (Bird 1982) were gina). The abrupt termination of the uterine folds killed within 48 h of artificial insemination. The ovi- observed macroscopically (Fig. 1) is seen by light mi- ducts were removed, immersed in toto into neutral croscopy as an abrupt cessation of the tubular glands buffered formalin (NBF), and stored (6-8 weeks) at (Fig. 2). No transitional forms of uterine tubular room temperature until processed. Whole oviducts glands or SST were observed. Sperm-storage tubules were transferred to Mirskey's fixative (National Di- were located in a band of UVJ mucosa about 3-4 mm agnostics) for about 24 h before gross dissection. For wide, indicated by the probe in Fig. 1. the precise localization and visualization of SST, the The surface epithelium at the UVJ is composed of connective tissue that binds the vagina in a tightly ciliated and nonciliated secretory cells, the latter ap- coiled structure between the uterus and the cloaca parently stained more intensely with PAS/H (Figs. was stripped. By carefully removing thin strips of 3-5). Serial sections of this region indicate that some connective tissue with fine forceps and scissors, the SST may be coiled, while others are relatively straight vagina was exposed and straightened. The vagina and tubular invaginations of the surface epithelium. The uterus were cut along the long axis of the oviduct epithelium around the SST orifice, and for a short and then pinned to a dissection board. The exposed distance into the SST, appears to be a continuation mucosa was kept moist with phosphate-buffered sa- of the UVJ surface epithelium (Fig. 5). There is an line (PBS). Individual mucosal folds were then re- abrupt transition between this epithelium and the 321 322 Short Communications [Auk, Vol. 104 .L-' Fig. 3. SST (arrows) subjacent to the PAS-positive Fig. 1. The uterine (U), uterovaginal junction surface epithelium. (PAS/H.) Bar = 50 (UVJ; probe), and vaginal (V) mucosae of F. sparve- ,m. rius. The probe points to the location of the band (3- 4 mm wide) of UVJ mucosa containing sperm-storage cessity of oviductal sperm storage in birds in general tubules. Bar = 2 mm. was addressed by Hatch (1983). Citing Lake (1975), Hatch (1983) noted that clutch size, mating system, epithelium lining the SST. The latter consists of non- and prevalence of renesting were factors that "... ciliated columnar cells that contain variable amounts may determine the selective value of oviductal sperm of a fine, granular PAS-positive material, possibly storage." He added a fourth factor, which he termed glycogen, in the supranuclear cytoplasm (Figs. 3-5). "delayed fertilization." Briefly, in this situation one No sperm were observed. individual (usually the female) leaves its partner af- Glandular grooves are located deep in the second- ter copulation to forage but returns to the nest site ary folds of the distal infundibulum (Fig. 6). The ep- before the onset of laying. ithelium that forms the glandular grooves contains We suggest that the function of oviductal sperm low columnar, nonciliated, PAS-negative epithelial storage must be considered in the context of the fate cells that form a slightly concave pocket. These struc- of sperm within the oviduct. The majority of sperm tures were shown to store sperm in the chicken (Van artificially inseminated are expelled from the vagina Drimmelen 1946, Fujii and Tamura 1963) and turkey within 1 h of insemination (Howarth 1971), and the (Bakst 1981) and generally are regarded as secondary UVJ acts as a barrier to adovarian sperm transport to the UVJ-SST with respect to sperm storage. Wheth- (Allen and Grigg 1957), permitting only viable sperm er they have the capacity to store sperm in the Amer- to enter the SST (Lake 1975). Also, sperm release from ican Kestrel is not known. the SST is either continuous or episodic during the Significance of oviductal sperm storage.-The breed- daily ovulatory cycle (Bakst 1981), but is reduced sig- ing behavior of the American Kestrel involves mul- nificantly when the hen is anovulatory (Bushman et tiple copulations before laying the first egg (Balgoo- al. 1985). Furthermore, an oviductal ovum depletes yen 1976). The role of the SST in the reproductive significantly the number of sperm within the ovi- process of the American Kestrel is not clear. The ne- ductal lumen (Bakst 1981). Finally, the time span in which the ovulated ovum is accessible to the sperm at the site of fertilization appears to be quite short, Fig. 2. The abrupt termination (arrow) of the uterine tubular glands (T) at the uterovaginal junc- Fig. 4. A section through the longitudinal axis of tion. This region corresponds to the region indicated two SST (arrows) to illustrate the coiled form of the by the probe in Fig. 1. Bar = 50 ,um. SST. Bar = 50 Mm. April 1987] Short Communications 323 7 T5 Fig. 5. The opening to the SST (arrow). (PAS Fig. 6. Slightly concave, PAS-negative, light- without counterstain.) Bar = 50 ,m. staining, glandular grooves (arrows) are deep in the secondary folds of the distal infundibulum. Bar = 50 because the deposition of oviductal secretory mate- Am. rial around the ovum, which begins at the distal in- fundibulum, renders the ovum impenetrable to sperm We acknowledge the support of the Natural Sci- (Bakst and Howarth 1977). We suggest that the SST ences and Engineering Research Council of Canada are necessary to ensure that a population of sperm and La Ministere du Loisir, de la Chasse, et de la adequate to maintain sustained fertility is present at Peche du Quebec.
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