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.     

Comparative analysis of the male reproductive accessory glands of bat species from the five Brazilian Subfamilies of the family Phyllostomidae (Chiroptera)

This study aimed to morphologically characterize and compare the male reproductive accessory glands (RAGs) of bats belonging to the five Brazilian subfamilies of the family Phyllostomidae (Carollia perspicillata—Carollinae; Desmodus rotundus—Desmodontinae; Glossophaga soricina—Glossophaginae; Phyllostomus discolor—Phyllostominae and Platyrrhinus lineatus—Stenodermatinae). The study demonstrated that the RAGs of phyllostomid bats were comprised of a pair of extra‐abdominal bulbourethral glands and an intra‐abdominal complex, composed of paraurethral glands and a prostate with two (Desmodontinae and Stenodermatinae) or three (Carollinae, Glossophaginae and Phyllostominae) different regions, with the absence of the seminal vesicles; this pattern possibly evolved from a process of compaction of the prostatic regions from an ancestor with three regions. J. Morphol. 276:470–480, 2015. © 2014 Wiley Periodicals, Inc.     

Larval development and metamorphosis of the olfactory and vomeronasal organs in the toad Rhinella (Bufo) arenarum (Hensel, 1867)

Jungblut, L.D., Pozzi, A.G. and Paz, D.A. 2010. Larval development and metamorphosis of the olfactory and vomeronasal organs in the toad Rhinella (Bufo) arenarum (Hensel, 1867). — Acta Zoologica (Stockholm) 92 : 305–315. The olfactory and the vomeronasal system are the two major chemosensory systems found in terrestrial vertebrates. Among tetrapods, amphibians are unique in having an aquatic larval stage, followed by metamorphosis to a terrestrial adult. In the present work, we studied the histological development of the olfactory and vomeronasal organ and associated multicellular glands of the toad Rhinella (Bufo) arenarum, from early poshatching larva to postmetamorphic toadlets. As in other bufonids, the olfactory epithelium of R. arenarum in larvae is divided into dorsal and ventral branches in the rostral and mid‐nasal regions. At metamorphic climax, the larval pattern changes drastically and the adult olfactory configuration develops. Bowman’s glands appear in the olfactory epithelium of R. arenarum at the onset of metamorphic climax. The vomeronasal epithelium develops early in larval development in R. arenarum, around the time of operculum development. Interestingly, a novel sensory epithelium develops in the floor of the principal chamber of R. arenarum at metamorphic climax. This novel sensory epithelium resembles larval sensory epithelium lacking Bowman’s glands, and suggests that these animals would be able to sense not only air‐borne, but also water‐borne odors during their adult terrestrial life.     

Anatomy and histology of the prostate and glands of Cowper in three species of neotropical bats

The reproductive accessory glands (RAG) are essential components in reproduction because their secretion products ensure survival, viability, and sperm motility. The objective of this study was to characterize and compare the morphological and histological structure of the RAG in three species of bats of the genus Sturnira (S. erythromos, S. lilium, and S. oporaphilum). The RAG complex comprise a compact gland (prostate), which surrounds the urethra, and a pair of Glands of Cowper at the base of penis. Anatomical and histologically, the prostate are differentiated in two regions, ventral and dorsal. The dorsal region has tubuloalveolar glands with secretions fine granular or accumulations of a gel‐like substance with bubbles and the ventral region, has alveolar glands with secretory cells form a single‐layer of small cells. The seminal vesicles are absent. The prostatic morphology of the three species is similar to that of other studied Stenodermatinae and Desmodontinae, but differs from other subfamilies of Phyllostomidae (Carollinae, Glossophaginae, and Phyllostominae) as that of Molossidae and Vespertilionidae. The RAG complex has no annual variation in relation to functionality or size, but it is variable depending on age (subadults and adults). This agrees with the annual reproductive pattern described for these species in these latitudes, where adult males are reproductively active throughout the year.     

Selective Eavesdropping Behaviour in Three Neotropical Bat Species

Knowledge of interspecies information transfer in mammals is scarce compared with other taxa. We investigated whether eavesdropping on echolocation calls of bats may be used by sympatric bats with similar feeding ecology. We performed playback experiments with three free‐ranging neotropical bat species, broadcasting search phase calls or feeding buzzes of conspecifics and heterospecifics belonging either to the same or to another bat family. Both the greater fishing bat Noctilio leporinus and the lesser bulldog bat Noctilio albiventris (Noctilionidae) reacted with repeated approaches in response to playbacks of search phase calls and feeding buzzes from conspecifics and also to congeneric feeding buzzes. Noctilio leporinus also were attracted by search phase calls from its sister species N. albiventris. In contrast, the sac‐winged bat Saccopteryx bilineata (Emballonuridae) did not react to any playback sequences presented. Our results support the existence of eavesdropping behaviour for both species of Noctilio. We suggest that information transfer via eavesdropping may depend mainly on species‐specific traits, including foraging style and social behaviour (territoriality, group foraging), and on distribution and density of prey. Call design had only a minor influence on the reaction.     

Evolutionary history of bulldog bats (genus Noctilio): recent diversification and the role of the Caribbean in Neotropical biogeography

We present phylogenetic relationships and phylogeographic patterns of the two species of bulldog bats, genus Noctilio. Using a comprehensive sampling of 118 individuals throughout the species distribution, we investigated the distribution of molecular variation in one nuclear and two mitochondrial markers. Phylogenetic trees do not recover Noctilio albiventris as a monophyletic group and point to three similar‐age intraspecific genetic lineages, suggesting cryptic diversity in this taxon. These lineages correspond to the subspecies previously proposed, and are strongly associated with major river basins in South America. Analyses also suggest a very recent origin for the fishing bat Noctilio leporinus, which probably originates from N. albiventris, with a population expansion corresponding to its invasion in South America. Based on our analysis, the speciation event was dated in the Pleistocene epoch and seems to be associated with the variation of the sea level in the Caribbean islands. The present work indicates how phylogeographic studies support the identification of independent evolutionary lineages, driving new systematic/taxonomic investigations, while at the same time shed light on the role of the Caribbean in shaping Neotropical bat fauna diversity. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Histology,ultrastructure, and seasonal variations in the bulbourethral gland of the African straw-colored fruit bat Eidolon helvum

We studied the morphological characteristics and seasonal changes of the bulbourethral gland of Eidolon helvum in a typical African tropical environment. Forty-eight bulbourethral glands were examined using gross anatomical, histological, histochemical, and ultrastructural techniques during the early rainy, late rainy, and peak dry seasons. The pear-shaped bilateral bulbourethral glands were located extra-abdominally in the inguinal region. Trabeculae from the capsule divided the parenchyma into numerous lobules of tubuloalveolar glandular acini. The mucosa was covered by a simple columnar epithelium consisting up of principal secretory cells, columnar dense cells and basal cells, which were progressively pronounced during the dry season. The principal cells contained eosinophilic granules, which were PAS positive while the dense cells did not show affinity for the stains. The mean gross weights, acini diameters, and epithelial heights were greater during the rainy season than the dry season. Ultrastructural evaluation showed that the cytoplasm of the principal cells contained well-developed Golgi complexes, rough endoplasmic reticulum, mitochondria, and secretory vesicles of varying electron densities and sizes. The secretory vesicles were numerous during the early rainy season, decreased during the late rainy season and were scanty during the peak dry season. The simple columnar epithelium observed during the rainy season was replaced by an undefined stratified epithelium during the dry season, and this was associated with cellular degenerations and regenerations. In conclusion, E. helvum has a typical mammalian bulbourethral gland, with a unique cell type, the dense cell whose functions are not well-understood. The gland exhibits cyclical seasonal variation in structure and secretory activity; being active during the early rainy season (breeding season), and showing the lowest activity during the dry season (non-breeding season). Glandular epithelial cell renewal occurs during the dry season in preparation for the next breeding season.     

The morphology of the dorsal and ventral skin of Triturus karelinii (Caudata: Salamandridae)

In this study, for the first time, the morphology of the dorsal and ventral skin of Triturus karelinii using light microscopy through histochemical methods was described. The skin exhibited basic morphological characteristics of the other urodeles: the epidermis composed of keratinized stratified epithelium with numerous conical protrusions and the dermis subdivided into spongy and compact layers. In the spongious dermis, three distinct types of glands were observed, namely serous, mucous and mixed glands. These glands were alveolar and occurred in both males and females. The morphologies of all three skin glands differed from anurans and other urodeles, having peculiar characteristics. Serous glands exhibited three different appearances. An unusual finding in mucous glands was the different appearance of their granules, showing diverse density after staining with PAS and AB. The histochemical analysis clearly demonstrated the presence of neutral, acid and sulfated mucins in the adenocytes of mucous glands. Mixed glands formed by mucous and serous glands exhibited the same morphological traits of both types of glands. Light microscopic observations revealed that the dorsal and ventral skin showed structural similarities with some minor differences, possibly resulting from their functions.     

New records of tree roosts of Noctilio albiventris from the Pantanal,Brazil

The selection of roosts is considered a critical factor to the survival of Noctilio albiventris. Thus, we located and identified N. albiventris day roosts in the Pantanal, near the Miranda River. We identified four species of tree: Banara arguta, Inga vera, Ocotea diospyrifolia and Vitex cymosa. Additional studies are important to understand the impact of specific requirements in the selection of roosts for Noctilio albiventris and to compare the observed patterns in different environments.     

The structure of the cutaneous pedal glands in the banded snail Cepaea hortensis (Müller, 1774)

Although gastropods have been crawling through the ocean and on the land for 60 million years, we still know very little about the sticky mucus produced in their foot. Most research has been focused on marine species in particular and, to a lesser extent, on the well‐known terrestrial species Arion vulgaris and Cornu aspersum. Within this study, we aim to characterize the foot anatomy of a smaller representative of the family Helicidae, the banded snail Cepaea hortensis. We are particularly interested in the microanatomy of the foot glands, their position, and the histochemical nature of their secretory content. Characterization of the dorsal foot region of Cepaea hortensis reveals four glands, differing in their size and in the granules produced. Histochemically, three of them react positively for sugars (PAS staining and lectin affinity tests for mannose, glucose and N‐acetyl‐d ‐glucosamine) and acidic proteins (positive Alcian blue and Toluidine blue staining), indicating the presence of acidic glycosaminoglycans. The fourth gland type does not react to any of these dyes. The ventral pedal region includes two different gland types, which are positive for the presence of acidic glycoproteins, with a lectin affinity for mannose only. A comparison with Helix pomatia indicates differences regarding the number of glands and their contents. In Helix, only three gland types are described in the dorsal region of the foot, which show a similar granular appearance but nevertheless differ in their chemical composition. Congruently, there are two gland types in the ventral region in both species, whereas in Helix an additional sugar moiety is found. This raises the question whether these differences between the pedal glandular systems of both helicid species are the result of protection or size‐related adaptations, as they occur in the same habitat.     

Functional morphology and neuronal innervation of the prothoracic defence gland in Timema

Timema is the most basal genus of Phasmatodea and the sister group to the remaining stick and leaf-insects (Euphasmatodea). An autapomorphy of all phasmids is the paired prothoracic exocrine defence glands. In this study, the anatomy and innervation of the defence glands in Timema petita and Timema chumash are described and compared with the data on Euphasmatodea. In all phasmids, the glands consist of a cuticular epithelium, a secretory epithelium and muscular fibres that compress the lumen. In Timematodea, the muscular part of the gland is less developed than in Euphasmatodea and the ejection of the defence secretion depends on the dorsal longitudinal neck muscles. On the neuroanatomical level, Timema petita and Timema chumash lack neurons that are involved in the independent contraction of the gland in euphasmids. In both studied species of Timema, neck muscles play an active role in the gland function which is not observed in any other phasmid. Considering the basal position of this genus, this supports the hypothesis that in euphasmids, the muscular part of the gland evolved from the dorsal longitudinal neck muscles. Additionally, the same nerves that innervate the dorsal longitudinal neck muscles in all Polyneoptera also innervate the defence glands in phasmids.     

Histochemical and quantitative study of the cloacal glands of Triturus marmoratus marmoratus (Amphibia: Salamandridae)

The cloacal glands of the male marbled newt Triturus marmoratus marmoratus were studied during winter and summer by histochemical and quantitative histologic methods. Four types of glands were distinguished: pelvic, dorsal, ventral, and Kingsbury's glands. The pelvic and dorsal glands have an eosinophilic epithelium and secrete neutral mucins. The ventral and Kingsbury's glands have a basophilic epithelium and secrete acid mucins. The lectin-histochemical characterization of the carbohydrates secreted by the four gland types revealed that the secretion of both the pelvic and Kingsbury's glands contain β-GalNAc in the peripheral region of the oligosaccharide, and that the dorsal glands secrete a glycoprotein with α-GalNAc. The ventral gland sections did not react to any of the lectins used here. The quantitative study revealed that the cloaca undergoes seasonal variations in volume, being significantly larger in winter than in summer. The total volume occupied by both the pelvic and ventral glands, as well as their tubular diameter, are also significantly greater in winter, while these parameters do not vary in dorsal and Kingsbury's glands. No seasonal differences were observed in the height of the epithelium in any gland     

Morphological comparison of the ampullae of Lorenzini of three sympatric benthic rays

This study investigated and compared the morphology of the electrosensory system of three species of benthic rays. Neotrygon trigonoides, Hemitrygon fluviorum and Maculabatis toshi inhabit similar habitats within Moreton Bay, Queensland, Australia. Like all elasmobranchs, they possess the ability to detect weak electrical fields using their ampullae of Lorenzini. Macroscopically, the ampullary organs of all three species are aggregated in three bilaterally paired clusters: the mandibular, hyoid and superficial ophthalmic clusters. The hyoid and superficial ophthalmic clusters of ampullae arise from both dorsal and ventral ampullary pores. The dorsal pores are typically larger than the ventral pores in all three species, except for the posterior ventral pores of the hyoid grouping. Ampullary canals arising from the hyoid cluster possessed a quasi‐sinusoidal shape, but otherwise appeared similar to the canals described for other elasmobranchs. Ultrastructure of the ampullae of Lorenzini of the three species was studied using a combination of light, confocal and electron microscopy. All possess ampullae of the alveolar type. In N. trigonoides and M. toshi, each ampullary canal terminates in three to five sensory chambers, each comprising several alveoli lined with receptor and supportive cells and eight to 11 sensory chambers in H. fluviorum. Receptor cells of all three species possess a similar organization to those of other elasmobranchs and were enveloped by large, apically nucleated supportive cells protruding well into the alveolar sacs. The luminally extended chassis of supportive cells protruding dramatically into the ampullary lumen had not previously been documented for any elasmobranch species.     

Anatomy and ultrastructure of dermal glands in an adult water mite,Teutonia cometes (Koch, 1837) (Acariformes: Hydrachnidia: Teutoniidae)

Organization of dermal glands in adult water mites Teutonia cometes (Koch, 1837) was studied using light-optical, SEM and TEM methods for the first time. These glands are large and occur in a total number of ten pairs at the dorsal, ventral and lateral sides of the body. The slit-like external openings of the glands (glandularia) are provided with a cone-shaped sclerite, and are combined with a single small trichoid seta (hair sensillum), which is always situated slightly apart from the anterior aspect of the gland opening. Each gland is formed by an epithelium encompassing a very large lumen (central cavity) normally filled with secretion that stains in varying intensity on toluidine blue stained sections. The epithelium is composed of irregularly shaped secretory cells with an electron-dense cytoplasm and infolded basal portions. The cells possess a large irregularly shaped nucleus and are filled with tightly packed slightly dilated cisterns and vesicles of rough endoplasmic reticulum (RER) with electron lucent contents. Dense vesicles are also present in the apical cell zone. Some cells undergo dissolution, occupy an upper position within the epithelium and have a lighter cytoplasm with disorganized RER. Muscle fibers are regularly present in the deep folds of the basal cell portions and may serve to squeeze the gland and eject the secretion into the external milieu. The structure of these dermal glands is compared with the previously described idiosomal glands of the same species and a tentative correlation with the glandularia system of water mites is given. Possible functions of the dermal glands of T. cometes are discussed.     

Fine structure of the male reproductive system in two species ofHaplognathia sterrer (Gnathostomulida,Filospermoidea)

Summary The structure of the male reproductive systems of two species ofHaplognathia cf.lyra andH. cf.rosacea was described. The structure of the testes and the anterior portions of the sperm ducts in both species was found to be similar. However, considerable species differences were found between the structures of the glands and muscles associated with the reproductive systems. These were more elaborate inH. cf.lyra than inH. cf.rosacea. The former species possessed an H-shaped sperm duct gland, three distinct groups of penis muscles and a penis with two cell types and with a lumen. The latter species had paired sperm duct glands, no specialized penis muscles and a penis with only one cell type and without a detectable lumen. No open gonopore was observed in either species. The sperm presumably exit through a ventral tissue connection observed connecting the penis and the ventral epidermis. These findings were discussed in the light of Mainitz's (1977) theory concerning the primitive penis type within the Gnathostomulida.Abbreviations ap anterior-posterior penis muscles - bm basement membrane - csd common sperm duct - dl dorsal lumen of the penis - dp dorsal gland cells of the penis - dv dorsoventral muscles anterior to the penis - dw sperm duct wall cell - e epidermis - ex exit cell - g intestine - gl gut lumen - n nerve - p penis - sd sperm duct - sdg sperm duct gland - tw testes wall cell - vl ventral lumen of the penis - vp ventral gland cells of the penis This project was supported by NSF grant #GB 42211 (R.M. Rieger P.I.). The line drawings have been executed after our design by Ms. Linda McVay     

The dorsal tail tubercle of Mertensiella caucasica and M. luschani (Amphibia: Salamandridae)

Males of the two species of Mertensiella (M. caucasica and M. luschani) possess a tubercle projecting from the skin of the dorsal tail base, the single morphological character that defines the genus. The dorsal tail tubercle functions during courtship, and its role is similar in both species. The tubercle is inserted into the cloaca of the female during ventral amplexus, shortly before the male deposits a spermatophore. Histological examination, however, revealed that the dorsal tubercles differ structurally between the two species. In M. caucasica, the tubercle consists primarily of elongate mucous glands, with granular glands occurring only at the base. Both mucous and granular glands of the tubercle are larger than those in typical skin. Unlike typical skin, however, mucous glands are larger than granular glands. In M. luschani, mucous glands and granular glands occur throughout the tubercle, and the granular glands are larger than the mucous glands, although both types are larger than those in typical skin. The dorsal tubercles of M. caucasica and M. luschani may not be homologous structures and may have resulted from convergent evolution. J Morphol 232:93–105, 1997. © 1997 Wiley-Liss, Inc.     

Characterization of the Arion vulgaris pedal gland system

The most common European gastropod species, Arion vulgaris, is one of the most troublesome pests for private garden owners and commercial agriculturists. The sticky and hard to remove secretion produced by these animals allows them to overcome most artificial and natural barriers. However, this highly adherent biopolymer has recently shown great potential for novel wound-healing applications in medicine. Nevertheless, our knowledge of the underlying gland system is still limited and few studies on the ventral gland system are available. We studied the lateral and ventral pedal glands in Arion vulgaris to determine their secretory content histochemically and through lectin assays. Using these histological and histochemical methods we differentiate five gland types with different mucus composition in the lateral pedal region of the foot of Arion vulgaris. These contain sulphated and carboxylated mucosubstances (positive Alcian blue staining) but lack hexose-containing mucosubstances (negative PAS staining). In the ventral pedal region, four gland types can be differentiated producing sulphated and carboxylated mucosubstances. Within the ventral mucus, a high affinity for the lectins PNA and WGA is observed. While the lateral glands are histochemically negative for PAS, a positive staining with the lectin JAC is observed. Arion vulgaris shows clear morphological differences from other arionid species. This raises the question whether the variation in the chemistry of the secretory material and mucus composition is the result of different functions and/or is related to the animals' different environmental conditions. A comparison of some glands of Arion vulgaris with those of the helicid species Helix pomatia and Cepaea hortensis indicates morphological similarities.     

Comparative histology of the digestive tract in three new world marsupials

We compare the main histological features of the digestive tract of three selected New World didelphid marsupials (Mammalia, Metatheria, Didelphimorphia, Didelphidae): the White-eared Opossum Didelphis albiventris Lund, 1840, the Short-tailed Opossum Monodelphis dimidiata Wagner, 1847, and the Patagonian Opossum Lestodelphys halli Thomas, 1921. The three species have a geographic distribution restricted to south-eastern and southern South America, and have quite distinct body masses, adaptations and life histories. Our observations include the following: (i) submucosal glands are present throughout the oesophagus of D. albiventris, only in its first third in M. dimidiata, and are lacking in L. halli; (ii) in the stomach and duodenum, the serus coat coat in D. albiventris is cuboidal (simple, squamous mesothelial layer in the other two species); (iii) the duodenum in L. halli has large folds, short crypts and Brunner's glands (the other species lack folds and Brunner's glands); (iv) the colon's mucous membrane has short, scarce villi in D. albiventris (villi absent in the remaining species). Some of the observed differences can be due to ecological adaptations, especially in the relatively large-sized, extremely omnivorous D. albiventris (e.g., colon villi).     

Morphological analysis of the female reproductive system of Stenorhynchus seticornis (Brachyura: Inachoididae) and comparisons with other Majoidea

We examined the female reproductive system of the yellowline arrow crab Stenorhynchus seticornis by means of histological and histochemical techniques. Mature specimens obtained in the field were kept in the laboratory for mating experiments. After 24 h, newly mated females were dissected, and their reproductive trait routinely processed for embedding in historesin. The specimens examined each possessed a pair of kidney‐shaped seminal receptacles (SR), and these we classified as ventral type, based on the location of the oviduct opening. The mesodermal dorsal region (DR) of SR consisted of a stratified epithelium with scaly cells, while the ectodermal ventral region (VR) was composed of a simple epithelium covered by a cuticle. The oviduct opened at the transition region (TR) between DR and VR and had no velum. The simple epithelium of TR had more folds on the face of the oviduct opening. The vagina exhibited the same features as the TR epithelium and was contiguous to VR, anchored by muscles. In the lumen, from one to three strata of sperm packets were observed, the dorsal one containing free sperm, and the most ventral stratum, spermatophores. An acidophilic glycoprotein layer enclosed the strata. Spermatophores in the ventral stratum were enclosed in a voluminous secretion, composed by acid polysaccharides most likely from the last male mated. The ventral‐type receptacle, stratified sperm packets, and polyandry, usually observed in females of Majoidea, suggest the occurrence of sperm competition in S. seticornis, favoring the sperm of the last male mated, as its sperm mass is located near the opening of the female oviduct.