Sperm Storage in a Tropical Nectar-Feeding Bat, Macroglossus minimus (Pteropodidae)

Abstract

Storage of spermatozoa in the mammalian female reproductive tract has been widely reported in shrews (Soricidae—Pearson, 1944), rodents (Muridae—Dewsbury, 1984; Ullman, 1976), hares (Leporidae—Martinet and Raynaud, 1975), and bats (Krishna and Dominic, 1978; Mori and Uchida, 1980; Mori et al., 1982; Racey et al., 1975). In this paper, we report the first example of sperm storage in the nectar-feeding bat Macroglossus minimus. These observations extend the occurrence of sperm storage in bats to a tropical, noninsectivorous species of the family Pteropodidae and raise questions about traditional explanations of this phenomenon in Chiroptera. Observations on sperm storage in Macroglossus minimus were based on specimens collected during the summer of 1979 and 1981 in Papua New Guinea. Samples were obtained from islands of the Bismarck Archipelago (Manus, New Britain, New Ireland, and Duke of York) and from Central Province, Papua New Guinea. Specific locality data were provided by Hood (1986). One hundred and forty female specimens were examined by gross anatomical dissection; reproductive tracts from 24 specimens were prepared by standard histological techniques tor light microscopic examination. Voucher specimens are deposited in the Division of Mammals, Natural History Museum of Los Angeles County. Spermatozoa were found in the uterine cornua of eight nonpregnant specimens of M. minimus. Stored spermatozoa were restricted to the gestational uterus and were not found within the vagina, cervix, oviduct, or uterotubal junction. Free spermatozoa were not found in any portion of the female reproductive tract. Spermatozoa were arranged consistently in parallel, their heads oriented toward the endometrium, forming an intimate contact with maternal epithelial cells (Fig. 1). In each specimen examined histologically, both ovaries contained undeveloped follicles; no specimens contained preovulatory (mature) follicles or corpora lutea. Together with observations on the distribution of attached spermatozoa, these data support the conclusion that these females possessed stored sperm. Elimination of spermatozoa from the female reproductive tract following fertilization apparently is extremely rapid. In specimens that contained unimplanted and early implanted blastocysts, no traces of intact tree or attached spermatozoa were observed. The uterine lumina in these specimens contained a small amount of cellular debris; numerous phagocytic cells were observed in the lumina and interstitial spaces. Because our material was prepared for light microscopic study only, we could not determine if elimination was through phagocytosis by leucocytes, maternal epithelial cells, or through some other mechanism of cellular disintegration. However, the observation of a dramatic increase in the numbers of phagocytic cells and amount of luminal debris following fertilization is consistent with elimination by leucocytic phagocytosis. In the order Chiroptera, sperm storage has been reported previously in 23 species of the families Vespertilionidae and Rhinolophidae (Fenton, 1984; Racey, 1979). The site of prolonged storage of spermatozoa in most bats is the oviduct or uterotubal junction. In M. minimus the site of storage is the gestational uterus; attached spermatozoa were absent from oviductal and cervical regions. Special morphological relationships between spermatozoa and maternal tissues, principally involving epithelial cells, have been observed in most chiropteran examples. Orientation and attachment of spermatozoa to uterine or oviductal epithelia has been described in many vespertilionid sperm-storing species (Krishna and Dominic, 1978; Medway, 1972; Mori and Uchida, 1974; Racey et al., 1975). In Myotis lucifugus and M. velifer studied by Krutzsch et al. (1982), the uterine corpus and cornua were filled with spermatozoa that had no special orientation or attachment, whereas sperm found in the uterotubal junction were attached firmly to oviductal epithelial cells. The morphological relationships of stored spermatozoa in Macroglossus minimus generally appear to be similar to those observed in other species of bats.