Ovulation, fertilization, and early embryonic development in the menstruating fruit bat, Carollia perspicillata.

To characterize periovulatory events, reproductive tracts were collected at 12 hr intervals from captive-bred, short-tailed fruit bats, Carollia perspicillata, on days 1-3 post coitum and examined histologically. Most bats bred readily. Graafian follicles developed large antra and exhibited preovulatory expansion of the cumulus oophorus. Ovulation had occurred in some on the morning, and in most by the evening, of day 1. The single ovum was released as a secondary oocyte and fertilized in the oviductal ampulla. Ovulated secondary oocytes were loosely associated with their cumulus cells, which were lost around the initiation of fertilization. Supernumerary spermatozoa were occasionally noted attached to the zonae pellucidae of oviductal ova, but never within the perivitelline space. By day 2, most ova had reached the pronuclear stage and by day 3, early cleavage stages. Several lines of evidence indicate that C. perspicillata is a spontaneous ovulator with a functional luteal phase. Most newly mated females had recently formed, but regressing corpora lutea, and thickened (albeit menstrual) uteri despite having been housed with males only for brief periods (<23 days). Menstruation is usually periovulatory in this species. Furthermore, the interval between successive estrus periods in most mated females that failed to establish ongoing pregnancies at the first was 21-27 days. Menstruation involved substantial endometrial desquamation, plus associated bleeding, and generally extended to the evening of day 3, the last time point studied. In nearly all females with a recent corpus luteum (n = 24 of 25; 96%), the preovulatory or newly ruptured follicle was in the opposite ovary.

Selectivity in the transport of spermatozoa to oviductal reservoirs in the menstruating fruit bat, Carollia perspicillata.

To better document the timing of ovulation and fertilization, female reproductive tracts were collected every 12 h from captive-bred fruit bats (Carollia perspicillata) on days 1-3 postcoitum and examined histologically. This also permitted observations on sperm transport, storage, and disposition. As the animals had previously been sexually segregated, most had been cycling and possessed menstrual uteri at the time of collection. Menstruation is periovulatory in this species. A widespread, headfirst orientation of spermatozoa to the uterine mucosa was observed in specimens apparently collected soon after insemination. Thereafter, however, this relationship was limited in most cases to the area around the entrance of each uterotubal junction (UTJ). A small number of spermatozoa also colonized the UTJs, which functioned as temporary sperm reservoirs on days 1-2. Although C. perspicillata is monovular, no consistent differences were observed between the two oviducts in the pattern of sperm storage and release. Very few sperm were ever observed in the isthmus or ampulla (the site of fertilization). Menstrual debris (including fine particulate matter) and leukocytes present in the uterine cavity in most tracts did not gain access to the UTJ with the spermatozoa. Smooth muscle and abundant elastic fibers in the wall of the intramural UTJ, as well as receptors on its luminal epithelial cells, may play roles in the selective transport of spermatozoa to the fertilization site. While some spermatozoa are phagocytosed in the uterine lumen or by epithelial cells in the UTJ, the fate of most is probably expulsion into the vagina.

Embryonic staging system for the short-tailed fruit bat, Carollia perspicillata, a model organism for the mammalian order Chiroptera, based upon timed pregnancies in captive-bred animals.

There are approximately 4,800 extant species of mammals that exhibit tremendous morphological, physiological, and developmental diversity. Yet embryonic development has been studied in only a few mammalian species. Among mammals, bats are second only to rodents with regard to species number and habitat range and are the most abundant mammals in undisturbed tropical regions. Bat development, though, remains relatively unstudied. Here, we describe and illustrate a staging series of embryonic development for the short-tailed fruit bat, Carollia perspicillata, based on embryos collected at timed intervals after captive matings. As Carollia can be readily maintained and propagated in captivity and is extremely abundant in the wild, it offers an attractive choice as a chiropteran model organism. This staging system provides a framework for studying Carollia embryogenesis and should prove useful as a guide for embryological studies of other bat species and for comparisons with other orders of mammals.

An ultrastructural study of interstitial implantation in captive-bred, short-tailed fruit bats, Carollia perspicillata: trophoblastic adhesion and penetration of the uterine epithelium.

Trophoblastic adhesion to, and penetration of, the uterine epithelium during implantation have been examined in captive-bred Carollia perspicillata at the light and electron microscopic levels. Initial adhesion is localized to marginal ridges immediately over the apical intercellular junctions of the epithelial cells. Penetration then involves the intrusion of trophoblastic processes between the epithelial cells and the formation of junctional complexes between the two cell types. As larger areas of adhesion develop, they still occur most often near the intercellular boundaries between the more flattened epithelial cells or on their lateral sides. This suggests that many (if not all) of these broad areas of adhesion to the trophoblast had actually formed along what had originally been part of the lateral (rather than the apical) surfaces of the epithelial cells. Portions of the apical cell surfaces further removed from their intercellular boundaries usually were not adherent to the trophoblast and still had microvilli. Upon reaching the basal lamina of the uterine epithelium, invasion of the endometrium is temporarily retarded, and trophoblast cells migrate instead between the basal lamina and the epithelial cells. This occurs extensively along both the luminal and glandular epithelia around the implantation site, but not significantly along their apical surfaces. This again indicates that adhesive interactions between the trophoblast and those apical surfaces are at most very limited in Carollia. The epithelial cells appear to be viable until separated from their basal laminae by the trophoblast. They are then phagocytized by the trophoblast. During initial penetration of the uterine luminal epithelium, the trophoblast is still entirely of the cellular variety. Syncytiotrophoblast does not begin to appear until later, when the trophoblast first comes into contact with endometrial capillaries.