Roosting Ecology of the Tent‐Roosting Bat Artibeus watsoni (Chiroptera: Phyllostomidae) in Southwestern Costa Rica1

We described the plants used as roost resources by Artibeus watsoni in southwestern Costa Rica, assessed roost fidelity, and compared roosting ecology between two sites, Golfito and Corcovado, which vary in the degree of human influence. A total of 349 tents from 25 different plant species were used by A. watsoni as roosts; some plant species (e.g., Carludovica palmata, Asplundia alata, Heliconia imbricata and Calathea lutea) were modified into tents with significantly higher frequency than others. The highest tents above the ground were observed in Philodendron popenoei and Rhodospatha wendlandii, whereas tents in Philodendron grandipes and A. alata were significantly lower than any other species. Asplundia alata and R. wendlandii also had the highest frequency of leaves modified per plant. Fidelity of bats to tents was low, although bats used several tents intermittently within a restricted area. Males generally were more faithful to tents than females, although not significantly so. This observation, along with indirect evidence of leaf modification, suggests that males are primarily responsible for tent construction. The two study sites differed in the plants used for roosting and in tent fidelity. Bats in Corcovado used a greater variety of plant species for tent roosting, whereas bats in Golfito were more faithful, suggesting that roosting resources were scarcer at the latter site.     

Roosting behavior and group stability of the big fruit-eating bat Artibeus lituratus (Chiroptera: Phyllostomidae)

The roosting behavior of the big fruit-eating bat, Artibeus lituratus (Phyllostomidae, Stenodermatinae) in an Andean region of Venezuela is described. Sixty-four video recordings made at three separate foliage roosts during 1 year showed that group size varied between two and 14 individuals. One male was regularly observed roosting with more females than others, and this male was associated with the highest quality roost, defined here as the highest, most structurally stable, and least disturbed. Males invariably occupied exclusive roosts during the study, whereas females frequently moved among adjacent roosts. The high roost fidelity of males appears to be related to the defense of the highest quality roosts. Because females were observed roosting with each of the three males present at the study site, female groups were considered unstable. We suggest that shuttling movements of individuals may reflect a commonly observed adaptation of foliage roosting bats related to the avoidance of predators and/or parasites. The type of male–female association observed in A. lituratus is consistent with a resource defense polygyny hypothesis.     

Morphological analysis of the male reproductive accessory glands of the bat Artibeus lituratus (Phyllostomidae: Chiroptera)

Bats are distributed worldwide from tropical to temperate regions. Despite their wide geographical radiation and advances in studies using evolutionary approaches, aspects related to the reproduction of these animals remain poorly explored, especially those related to the male reproductive accessory glands (RAGs). Thus, the aim of this study was to analyze the morphophysiology of the male RAGs in the bat Artibeus lituratus. The RAGs in A. lituratus are composed of a compact intra‐abdominal glandular complex, consisting of the prostate with two prostatic regions (ventral and dorsal), plus Littre glands and a pair of extra‐abdominal bulbourethral glands. The ventral region of the prostate has an epithelium with variable morphology, due to its holocrine type of secretion. In contrast, the dorsal region has a typical cubic‐to‐columnar pseudostratified epithelium. Both regions contain two cell types, basal and secretory cells. Similar to the epithelial morphology, the secretion also varies, with the ventral region containing numerous PAS‐positive globular vesicles, whereas the dorsal region has a more fluid, hyaline and PAS‐negative secretion. Littre glands are dispersed in the connective tissue of the urethra, while the bulbourethral glands are located in the penile root, both glands with cubic‐to‐columnar pseudostratified epithelium and globular PAS‐positive secretion. The results demonstrate that the RAGs of A. lituratus are composed of two prostatic regions, ventral and dorsal, and urethral and bulbourethral glands, with no seminal vesicles. Each prostatic region has unique and distinctive characteristics, with the ventral region presenting an exclusive holocrine nature and the dorsal region having similarities to the ventral prostate of rodents.     

Reproduction of the large fruit-eating bat Artibeus lituratus (Chiroptera: Phyllostomidae) in a Brazilian Atlantic forest area

In this study we investigated the male testicular activity and the reproductive condition of females in relation to their external reproductive characteristics (pregnant, lactating, post-lactating) in the phyllostomid bat Artibeus lituratus (Olfers, 1818). Five hundred and twenty six individuals were examined (197 males and 329 females) in the period December 2001 to May 2003. Throughout the study most males displayed large scrotal testes. Thirty-three males were randomly selected for histological examination at various times throughout the year and were found to have spermatogenic testes. The reproductive characteristics of the females indicated that they were reproductively active mainly during the wet season. Pregnancy occurs at the end of the dry season and parturition in the wet season. Most individuals captured after this season, mainly the females, were sexually immature. Our results suggest a seasonal monoestrous reproductive pattern for the species; however, adult males being fertile throughout the year could suggest polyoestry. Seasonal polyoestry is a possibility. There was, however, no evidence that females had more than one pregnancy per year.     

Male dominance,paternity, and relatedness in the Jamaican fruit-eating bat (Artibeus jamaicensis)

We analysed variation at 14 nuclear microsatellite loci to assess the genetic structure, relatedness, and paternity of polygynous Jamaican fruit-eating bats. A total of 84 adults captured in two caves exhibited little genetic differentiation between caves (FST = 0.008). Average relatedness among adult females in 10 harem groups was very low (R = 0.014 +/- 0.011), providing no evidence of harem structure. Dominant and subordinate males shared paternity in large groups, while dominant and satellite males shared paternity in smaller groups. However, our results suggest that male rank influences paternity. Dominant males fathered 69% of 40 offspring, followed by satellite (22%) and subordinate males (9%). Overall adult male bats are not closely related, however, in large harem groups we found that subordinate and dominant males exhibited relatedness values consistent with a father-offspring relationship. Because dominant and subordinate males also sired all the pups in large groups, we propose that their association provides inclusive fitness to them.     

Novel long-distance movements by Neotropical bats (Mammalia: Chiroptera: Phyllostomidae) evidenced by recaptures in southeastern Brazil

We report recapture data for phyllostomid bats in different types of forests, and at different altitudes, obtained through long-term fieldwork in southeastern Brazil. We provide evidence of long-distance movements, with bats moving up to 120 km from mountains to the beach, with an altitudinal variation of 1,237 m. These movements demonstrate the high mobility of these bats and represent the longest distances recorded for them so far in the Neotropics, besides reinforcing the need for long-term capture and recapture programs aimed at understanding the movement dynamics of bat populations.     

mtDNA perspective of chromosomal diversification and hybridization in Peters' tent-making bat (Uroderma bilobatum: Phyllostomidae)

We compared sequence variation in the complete mitochondrial cytochrome-b gene with chromosomal and geographical variation for specimens of Peters' tent-making bat (Uroderma bilobatum). Three different chromosomal races have been described in this species: a 2n = 42 race from South America east of the Andes, a 2n = 44 from NW Central America and 2n = 38 from the rest of Central America and NW South America. The deepest nodes in the tree were found within the South American race (42 race), which is consistent with a longer history of this race. Average distance among races ranged from 2.5 to 2.9%, with the highest amount of intraracial variation found within the 2n = 42 race (1.7%), intermediate values within the 2n = 38 race (0.9%) and lowest within the 2n = 44 race (0.5%). Variation among chromosomal races accounted for over 55% of molecular variance, whereas variation among populations within races accounted for 6%. The 2n = 38 and 2n = 44 races hybridize in the coastal lowlands of Honduras, near the Gulf of Fonseca. Introgression between these two races is low (two introgressed individuals in 45 examined). Clinal variation across the hybrid zone for the cytochrome-b of U. bilobatum, is similar to clinal variation reported for chromosomes and isozymes of this species. Mismatch distribution analyses suggests that geographical isolation and karyological changes have interplayed in a synergistic fashion. Fixation of the alternative chromosomal rearrangements in geographical isolation and secondary contact is the most likely mechanism accounting for the hybrid zone between the 2n = 38 and 2n = 44 races. If a molecular clock is assumed, with rates ranging from 2.3 to 5.0% per million years, then isolation between these races occurred within the last million years, implying a relatively recent origin of the extant diversity in Uroderma bilobatum. None the less, the three chromosomal races probably represent three different biological species.     

Reproductive biology of captive Arabian oryx (Oryx leucoryx) in Saudi Arabia

Reproductive data on captive Arabian oryx (Oryx leucoryx) were collected from June 1986 through April 1992 at the National Wildlife Research Center (Taif, Saudi Arabia). Oryx females are polyestrous. The estrous cycle averaged 22 days and mean gestation length was 260 ± 5.5 days (S.D). Sex ratio at birth was unbiased and mean weight was 6.5 ± 0.7 kg (S.D.), with no difference between sexes. Under captive breeding conditions, births occurred throughout the year. Females gave birth to a single calf at any time during the day and produced 1.03 young per year. Abortion rate was 3.6%. Mortality rate of young was 6.1% before weaning at 3 months of age. The interbirth interval averaged 295 ± 42 days (S.D.), with 53% lasting between 270 and 279 days. Females reached sexual maturity at the age of 13 months. © 1996 Wiley-Liss, Inc.     

Reproductive biology of the female little mastiff bat, Mormopterus planiceps (Chiroptera: Molossidae) in southeast Australia

The reproductive biology of the female little mastiff bat (Mormopterus planiceps) was studied from specimens obtained throughout the year in southeast Australia, within the region occupied only by the long penile form of this species. Mormopterus planiceps appeared to undergo a single pregnancy each year and was monotocous. Conception occurred during late winter/early spring after a protracted proestrus, during which the uterine/vaginal epithelia attained an extraordinary thickness; spermatozoa were present in the uterine corpus, vagina, and intramural oviduct for at least 2 months prior to ovulation, although only those present in the oviducts were entire and thus appeared to be viable. Following ovulation, a massive postovulatory infiltration of phagocytes occurred; and the thickness of the uterine corpus epithelium was dramatically reduced. As in other molossids, the tract was bicornuate and dextrally functional. The length of gestation was difficult to determine because early embryonic stages, up to implantation, appeared to span several months (late July/August/September) as did parturition (December/January). Growth of the young was slow; nevertheless, females attained sexual maturity in their first year. Several unusual features included the presence of a long os clitoridis, and tubuloalveolar sudoriferous and associated lobulated, sebaceous, paravaginal glands, which surrounded and emptied into the lower vagina. A deep fornix anterior and lateral to the cervix probably serves to receive the secondary glans penis. The epithelium of the uterine corpus was stratified and indistinguishable, in its cytology and cyclicity, from that of the vagina; furthermore, it lacked a glandular endometrium. This portion of the female tract likely receives the elongated primary glans. These findings are discussed in relation to other Molossidae and to the reproductive biology of male M. planiceps. Although the number of animals sampled was relatively small, the data suggest that this species does not exhibit the usual temperate molossid pattern of late winter/spring coincidence of spermatogenesis and ovulation. It would seem that pregnancy may begin, at least in some individuals, during the inhospitable winter months (when epididymal and uterine spermatozoa are abundant but spermatogenesis has largely terminated) and that additional conceptions continue into the early spring. The occurrence of sperm storage in both sexes of this species is unique among Molossidae studied to date.     

Population dynamics of the bat Dermanura tolteca (Chiroptera: Phyllostomidae) in a tropical forest in Mexico

The fruit-eating bat, Dermanura tolteca, has a broad geographic distribution in Mexico and it is a very important seed dispersal of Neotropical plants. Nonetheless, information on the biology of this bat species is scarce, especially with regard to demography. We studied some ecological aspects and population dynamics of D. tolteca from Southeastern Mexican State of Oaxaca. The study was conducted in a perennial tropical forest, over a period of 80 nights, a sampling effort of 73 200 mist-net-hour, from May 2006 to August 2007. A total of 176 specimens were captured, 98 females and 78 males. Population size was estimated in 237 individuals in the study area, with a greater number during rainy season. The population density of this bat, in its range of distribution in Mexico is low compared to other nose-leaf bats. Captures were correlated with monthly precipitation, and this result may be linked to food resources abundance in tropical and subtropical areas. The reproductive pattern was bimodal polyestrous, with birth periods between August-September and April-June. Greater body mass was observed in females than males. The male-female ratio and age-related demographics were similar to other nose-leaf bats. The biological characteristics of D. tolteca are typical of nose-leaf bats of the family Phyllostomidae.     

Fruit digestion time,integrity and germination of seeds defecated by Artibeus lituratus (Olfers, 1818) (Chiroptera: Phyllostomidae)

We evaluated the effects on the integrity, germinability and mean germination time of three Ficus species eaten by Artibeus lituratus in captivity. The passage of seeds through the digestive tract of the animal did not interfere in the germinability and the mean germination time of F. organensis; however, it increased the germination of F. guaranitica and reduced the mean germination time of F. glabra. The mean time of digestion of A. lituratus presented no significant difference for Ficus species. The results showed that A. lituratus has a good potential for dispersal and can modify the germination of some Ficus species.     

Visual acuity,sensitivity and binocularity in a gleaning insectivorous bat,Macrotus californicus (Chiroptera: Phyllostomidae)

Behavioural tests were used to examine the visual acuity and sensitivity of Macrotus californicus, a 12–14-g desert bat known to use vision in the location of terrestrial prey. Optomotor responses indicate single point visual acuity as fine as 3′38″ of arc. For comparison, the same tests were applied to two other species of bats. Antrozous pallidus, a desert gleaner which locates prey by the sounds they produce, exhibited acuity of 15′ of arc, and Eptesicus fuscus, an aerial foraging species that uses echolocation to find prey, 60′ of arc. Both M. californicus and A. pallidus retained their acuity at light levels as low as 2×10⁻⁴ mL (approximately 2×10⁻³ lux), comparable to ground luminance on a clear, moonless night. The eyes of M. californicus were more anteriorly directed, and had twice the binocular overlap of the other species examined. Comparison of our data with results from other studies indicate that M. californicus has vision superior to other insectivorous bats, and at least equivalent to larger-eyed frugivorous and nectarivorous bats examined in previous studies.     

Reproductive biology of the male little mastiff bat, Mormopterus planiceps (Chiroptera:Molossidae), in southeast Australia

The anatomy, biology, and chronology of reproduction in the male of the long penile form of Mormopterus planiceps was studied in southeast South Australia and Victoria. In the morphology of its primary and accessory reproductive organs, M. planiceps was generally reminiscent of other Molossidae; however, in the specialized (sebaceous) nature of the Cowper's gland ducts, in the presence of para-anal glands, and in the unusual, horizontally bifid glans penis and the greatly elongated os penis, it was distinct from other Molossidae studied to date. Young of the year were not reproductively active. Adults displayed a single annual spermatogenic cycle that commenced in spring (September/October) and culminated in spermiogenesis in autumn (February-May), during which period plasma levels of testosterone overtook androstenedione. Thereafter, spermatogenesis appeared to cease (though scattered sperm were seen in the seminiferous tubules until August), but abundant epididymal sperm reserves persisted until September/(October). The accessory glands were hypertrophied during this period, becoming involuted by October. Although the numbers of animals available for study were small, these observations, together with the appearance of spermatozoa in the ductus deferens in August/September suggested that mating could occur during the interval from autumn to spring. Late winter/spring insemination is normal for molossids from temperate environments. However, protracted spermatogenesis commencing in spring that is not accompanied by the availability of spermatozoa until autumn, and a subsequent apparent extension of fertility (epididymal sperm storage, accessory gland hypertrophy) beyond the testicular gametogenic phase, are aspects of the male reproductive cycle in M. planiceps that have not heretofore been described in another molossid bat.     

Impact of the processes of testicular regression and recrudescence in the prostatic complex of the bat Myotis nigricans (Chiroptera: Vespertilionidae)

Myotis nigricans is a species of vespertilionid bat, whose males show two periods of total testicular regression during the annual reproductive cycle in the northwest São Paulo State, Brazil. Thus, the aim of this study was to investigate the impact of total testicular regression on the prostatic morphophisyology and its regulation. The prostatic complex (PC) of animals from the four periods of the reproductive cycle (active, regressing, regressed, and recrudescence) was analyzed by different histological, morphometric, and immunohistochemical procedures to characterize its variations, analyze its hormonal regulation and evaluate whether the prostate is affected by the processes of testicular regression and recrudescence. The results indicated a decrease in the prostatic parameters from the active to regressed periods, which are related to decreases in the testicular production of testosterone and in the prostatic expression of androgen receptor (AR), estrogen receptor α (ERα) and aromatase. However, in regressed‐recrudescence periods, the prostatic expression of AR, ERα and aromatase increased, indicating the reactivation of the PC. Despite this, the PC appears to have a slower reactivation and seems not to follow the testicular recrudescence in morphological and morphometric terms. With these data, we demonstrate that the prostatic physiology is directly affected by total testicular regression and conclude that it is regulated by testosterone and estrogen, via the production of testosterone by the testes, its conversion to dihydrotestosterone by 5α‐redutase and to estrogen by aromatase, and the activation/deactivation of AR and ERα in epithelial cells, which regulate cell expression and proliferation. J. Morphol. 276:721–732, 2015. © 2015 Wiley Periodicals, Inc.     

Ultrastructure of spermatogenesis in the short‐tailed fruit bat,Carollia perspicillata (Chiroptera: Phyllostomidae: Carollinae)

Among species of the Chiroptera, spermatogenesis and the fully differentiated spermatozoa differ in morphological and ultrastructural detail. This study therefore aimed to ultrastructurally characterize the spermatogenesis and the spermatozoa of Carollia perspicillata (Phyllostomidae) and compare the process with other species of bats and mammals. The differentiation of spermatogonia is similar to other bats and to Primates, with three main spermatogonia types: A_d, A_p, and B. Meiotic divisions proceed similarly to those of most mammals and spermiogenesis is clearly divided into 12 steps, in the middle of the range of developmental steps for bats (9–16 steps). The process of acrosome formation is similar to that found in Platyrrhinus lineatus, with the acrosome formed by two different types of proacrosomal vesicles. The ultrastructure of the spermatozoon is similar to other bats already described and resembles the typical mammalian sperm model; however, its morphology differs from other mammals such as marsupials and rodents, on account of a simpler spermatozoon head morphology, which indicates a pattern that is more closely related to the sperm cells of humans and other primates. Our data demonstrated that spermatogenesis in C. perspicillata presents great ultrastructural similarities to P. lineatus. This pattern is not surprising, because both species belong to the same family (Phyllostomidae); however, it is observed that C. perspicillata presents some characteristics that are more closely related to phylogenetically distant species, such as Myotis nigricans (Vespertilionidae), which is a fact that deserves attention. J. Morphol. 275:111–123, 2014. © 2013 Wiley Periodicals, Inc.