Morphological and Histological Variations of the Reproductive Organs During the Annual Cycle in a Neotropical Bat: Peters' Ghost-Faced Bat Mormoops megalophylla (Chiroptera: Mormoopidae)

Abstract

Recent studies have emphasized the ecological significance of bats as insect regulators. This recognition has prompted an increased scientific interest in Mormoops megalophylla, a notable neotropical insectivorous bat species. The extant literature on its biology remains limited and substantial knowledge gaps persist, particularly regarding its reproductive cycle. This study sought to examine morphological and histological variations in the reproductive organs of male and female M. megalophylla over the annual cycle to elucidate the stages of its reproductive process. Over the course of the year, five sexually mature individuals of each sex were sampled monthly, culminating in a total of 120 specimens, to document variations in external sexual characters, the testes, epididymides, uterus, and ovaries; all sampled individuals underwent morphological, morphometric, and histological analyses. The findings indicate that M. megalophylla has migratory testes with seasonal spermatogenesis occurring from October to December, a bicornuate uterus, and a single folliculogenic period that is synchronized with spermatogenesis. This suggests a monoestrous, seasonal, and synchronous reproductive pattern. At the population level, copulation occurs between November and December, gestation occurs between December and May, and parturition occurs between late May and early June. The lactation period extended from June to September.

Keywords: biology; folliculogenesis; reproduction; sinistral dominance; spermatogenesis.

Figure 1

Map illustrating the research site (denoted by a yellow star) and documented occurrences of Mormoops megalophylla (represented by red dots) within the neotropical region (shaded in gray).

Figure 2

Precipitation levels (mm) recorded in the study area between April 2016 and March 2017.

Figure 3

Schematic diagram illustrating the morphometric analysis of the reproductive organs of Mormoops megalophylla. (A) Uterine measurements: width (a) and length (b) of the uterus, length of the right uterine horn (c) and length of the left uterine horn (d). (B) Embryonic measurements: width (e) and length (f) of embryos. (C) Epididymal measurements: length (g). (D) Testicular measurements: length (h) and width (i) of testes.

Figure 4

Reproductive cycle of Mormoops megalophylla in the cave “El Vado de la Chachalaca,” Carrizal, Veracruz, Mexico. (A) Active seminiferous tubule, (B) epididymis with spermatozoa, (C) male reproductive tract during the period of reproductive activity, (D) uterus at the initiation of gestation, (E) corpus hemorrhagicum (ovulation), and (F) embryo at the terminal stage of gestation. The rainy season is indicated here.

Figure 5

Ventral view of genital organs in the male bat Mormoops megalophylla. (A) External anatomy and, following skin removal, during the nonbreeding season in June (B) and February (C), and during the breeding season in October (D). B, bladder; E, epididymis; F, adipose tissue; G, glans; P, penis; PT, prostate; T, testicles.

Figure 6

Histological sections of the testis and epididymis of Mormoops megalophylla during different reproductive stages. (A) Corresponds to the reproductive activity phase in December; A1 shows active seminiferous tubules, and A2 shows an epididymis with sperm. (B) Corresponds to the reproductive inactivity phase in May; B1 shows inactive seminiferous tubules, and B2 shows an empty epididymis. E, epididymis; IT, interstitial tissue; L, lumen; SPZ, sperm; Staining, hematoxylin–eosin; TA, tunica albuginea; TS, seminiferous tubule.

Figure 7

Histological sections of the testis and epididymis of Mormoops megalophylla at different months of the reproductive cycle. Active reproductive stage: October (A and B) and December (C and D). Inactive reproductive stage: May (E and F) and June (G and H). ES, elongated spermatids; L, lumen; LC, Leydig cells; P, principal cells; SC, spermatocytes; SG, spermatogonia; SP, spermatids; Staining, hematoxylin–eosin.

Figure 8

Female reproductive apparatus of Mormoops megalophylla. (A) Long bicornuate uterus illustrating its general structure. Pelvic area where the embryo is observed during the gestational period in the months of (B) February, (C) April, and (D) May. B, bladder; E, embryo; K, kidney; LH, left uterine horn; P, placenta; RH, right uterine horn.

Figure 9

Histological sections of the left ovary of Mormoops megalophylla during (A) the onset of reproductive activity and (B) lactation. 1F, primary follicle; AF, follicle in atresia; AF1, advanced primary follicle; BV, blood vessels; GLC, granulosa luteal cells; HB, hemorrhagic body; LC, corpus luteum; PF, primordial follicles; Staining, hematoxylin–eosin; TLC, theca luteal cells.

Figure 10

Histological sections of ovarian follicles and luteal bodies in Mormoops megalophylla. (A) primordial follicle, (B) primary follicle, (C) advanced primary follicle, (D) atretic follicle, (E) hemorrhagic body, (F) corpus luteum. AF, atretic follicle; CFC, cuboidal follicular cells; FFC, flattened follicular cells; GC, granulosa cells; GLC, granulosa lutein cells; HB, hemorrhagic body; OC, oocyte; Staining, hematoxylin–eosin; TLC, thecal lutein cells; ZP, zona pellucida.

Figure 11

External morphology of the nipple in Mormoops megalophylla females during different reproductive stages. (A) Enlarged and protruding nipple during lactation, (B) reduced nipple in the post‐lactation stage, (C) small, inactive nipple outside the reproductive period. The arrows indicate the position of the nipple in each stage.