Gular Glands Research Articles

Comparative study of the gular gland of three species of Molossidae bats (Mammalia: Chiroptera) from South America.

The gular gland is a skin gland located in the suprasternal region of adult males of some bat families. Knowledge of the morphology and functional aspects of these gland types is often limited. This study aimed to describe the structure and composition of the gular glands of three molossid species (Eumops patagonicus, Molossus fluminensis and Molossus molossus) with respect to their reproductive activity and to define the mechanism involved in secretion release. Different histological, histochemical and immunohistochemical techniques were used to achieve these goals. The results revealed that the size and composition of this gland are variable and are mostly related to the lipid content during the reproductive season. The results also documented, for the first time, the occurrence of mechanoreceptors associated with the surface of the glandular duct by detecting an S100 protein, indicating that an external stimulus activates secretion. Previous studies on other species have classified the gland using obsolete criteria; hence, we adopted a new classification of adenomeres in this study. Moreover, we investigated the gland secretion mechanism previously proposed. This study defines the implications of this gland in the reproduction of this species. Our preliminary interpretation of the function of the gular gland is that it is a cutaneous exocrine gland activated by mechanoreceptors involved in the reproductive behaviour of the Molossidae family.

Identification and determination of the absolute configuration of amorph-4-en-10β-ol, a cadinol-type sesquiterpene from the scent glands of the African reed frog Hyperolius cinnamomeoventris.

Hyperolid reed frogs are one of the few families of Anurans known to possess glands that emit volatile compounds used in chemical communication. Hyperolius cinnamomeoventris, a model species, possesses a gular gland on its vocal sac that emits chemicals, and sends visual and auditory signals during calling. Previous investigations have shown that the glandular compounds are typically macrocyclic lactones. However, in this work, we show that another major constituent of the male specific gland is (10R,1S,6R,7R,10R)-amorph-4-ene-10β-ol [(1R,4R,4aR,8aS)-4-isopropyl-1,6-dimethyl-1,2,3,4,4a,7,8,8a-octahydronaphthalen-1-ol]. This compound was synthesized for the first time and has the opposite configuration to amorph-4-ene-10β-ol known from plants. A short synthesis using an organocatalytic approach through a tandem Mannich/intramolecular Diels-Alder reaction led to a mixture of cadinols, which was used for the assignment of the natural cadinol structures and their stereoisomers.

Cinnamomeoventrolide – Double Bond Regioisomerism in Frog Semiochemicals

Frogs of the families Mantellinae and Hyperoliidae possess male specific femoral or gular glands that are used during courtship. These glands release volatile compounds, e. g. the macrocyclic lactone gephyromantolide A (2,6,10-trimethyl-6-undecen-11-olide) in the case of Gephyromantis boulengeri (Mantellinae). During the analysis of the volatiles of Hyperolius cinnamomeoventris (Hyperoliidae) we detected an unknown compound A, which we called cinnamomeoventrolide, whose mass spectrum showed high similarity with the spectrum of gephyromantolide A. Nevertheless, slight spectral differences led to the proposal of a regioisomer of gephyromantolide A as a structure for A, 2,6,10-trimethyl-5-undecen-11-olide. A versatile synthesis of this compound was developed to allow access to all four stereoisomers from a single chiral starting material, the so-called (S)-Roche ester, using ring-closing metathesis as a key step. With these stereoisomers, the absolute configuration of the natural product was established to have the (2R,10S)-configuration by GC on a chiral phase. The configuration of natural gephyromantolide A is the opposite. Both frogs seem to use a similar biosynthetic pathway to access the target compounds, differing in the stereochemistry of the reduction steps, and requiring an additional isomerization in case of G. boulengeri. This unique regioisomeric differentiation of double bonds in semiochemicals has so far only been observed in insects. The compounds are likely to play a role in species-recognition of the frogs.

Multimodal Signal Testing Reveals Gestural Tapping Behavior in Spotted Reed Frogs.

In the majority of anuran species, acoustic signals are the dominant mode of inter- and intrasexual communication. Male calls are always accompanied by the movement of a more or less conspicuous vocal sac-a potential visual cue. Reed frogs possess a striking vocal sac with a colorful patch of gland tissue clearly visible once the vocal sac is inflated during acoustic signaling. To investigate the visual signal function of vocal sac and gular gland, we presented male Spotted Reed Frogs (Hyperolius puncticulatus) with unimodal and multimodal signal playbacks of conspecific rivals in their natural habitat and recorded their behavioral responses. We found no difference in receiver response to unimodal advertisement call stimuli and to multimodal stimulus presentations of calls combined with visual signals of an artificial vocal sac with or without a gular patch, moving synchronously or asynchronously with the call playback. The inflations of a vocal sac with a colorful gular patch did not alter receiver response and neither increase nor decrease signal salience during male-male communication. Interestingly, males frequently displayed a novel hind and front foot-tapping behavior in response to all playbacks. Comparison of male responses to advertisement and aggressive call playbacks showed that Spotted Reed Frogs approached the sound source less during aggressive call presentations. Tapping behavior was not influenced by either call playback. We suggest that the gestural tapping behavior might act as vibrational signal and discuss its potential signal function in male contests and courtship for females.

Frogolide - An Unprecedented Sesquiterpene Macrolactone from Scent Glands of African Frogs.

Some amphibians use chemical signals in addition to optical and acoustical signals to transmit information. Males of mantellid frogs from Madagascar and hyperoliid frogs from Africa emit complex, species- and sex-specific bouquets of volatiles from their femoral or gular glands. We report here on the identification, synthesis, and determination of the absolute configuration of a macrocyclic lactone occurring in several species of both families, (S)-3,7,11-dodec-6,10-dien-12-olide (S-14, frogolide). Macrolides are a preferred compound class of frog volatiles. Nevertheless, frogolide is the first macrocyclic lactone obviously derived from the terpene pathway, in contrast to known frog macrolides that are usually formed via the fatty acid biosynthetic pathway.

Identification, synthesis and mass spectrometry of a macrolide from the African reed frog Hyperolius cinnamomeoventris.

The contents of the gular glands of the male African reed frog Hyperolius cinnamomeoventris consist of a mixture of aliphatic macrolides and sesquiterpenes. While the known macrolide gephyromantolide A was readily identified, the structure of another major component was suggested to be a tetradecen-13-olide. The synthesis of the two candidate compounds (Z)-5- and (Z)-9-tetradecen-13-olide revealed the former to be the naturally occurring compound. The synthesis used ring-closing metathesis as key step. While the Hoveyda–Grubbs catalyst furnished a broad range of isomeric products, the (Z)-selective Grubbs catalyst lead to pure (Z)-products. Analysis by chiral GC revealed the natural frog compound to be (5Z,13S)-5-tetradecen-13-olide (1). This compound is also present in the secretion of other hyperoliid frogs as well as in femoral glands of male mantellid frogs such as Spinomantis aglavei. The mass spectra of the synthesized macrolides as well as their rearranged isomers obtained during ring-closing metathesis showed that it is possible to assign the location of the double bond in an unsaturated macrolide on the basis of its EI mass spectrum. The occurrence of characteristic ions can be explained by the fragmentation pathway proposed in the article. In contrast, the localization of a double bond in many aliphatic open-chain compounds like alkenes, alcohols or acetates, important structural classes of pheromones, is usually not possible from an EI mass spectrum. In the article, we present the synthesis and for the first time elucidate the structure of macrolides from the frog family Hyperoliidae.

Take time to smell the frogs: vocal sac glands of reed frogs (Anura: Hyperoliidae) contain species-specific chemical cocktails

Males of all reed frog species (Anura: Hyperoliidae) have a prominent, often colourful, gular patch on their vocal sac, which is particularly conspicuous once the vocal sac is inflated. Although the presence, shape, and form of the gular patch are well-known diagnostic characters for these frogs, its function remains unknown. By integrating biochemical and histological methods, we found strong evidence that the gular patch is a gland producing volatile compounds, which might be emitted while calling. Volatile compounds were confirmed by gas chromatography–mass spectrometry in the gular glands in 11 species of the hyperoliid genera Afrixalus, Heterixalus, Hyperolius, and Phlyctimantis. Comparing the gular gland contents of 17 specimens of four sympatric Hyperolius species yielded a large variety of 65 compounds in species-specific combinations. We suggest that reed frogs might use a complex combination of at least acoustic and chemical signals in species recognition and mate choice.

Salivary glands in Cicadidae (Hemiptera: Cicadoidea): comparative morphology, ultrastructure, and their phylogenetic significance

The present investigation provides information on gross morphology and ultrastructure of salivary glands of species in Cicadidae in detail. The structure of the salivary glands of 11 representative species from 10 genera belonging to three subfamilies of Cicadidae was studied using light microscopy and transmission electron microscopy. In the examined species, the salivary glands are paired structures, and each of which is comprised of a principal gland (pg) and an accessory gland (ag). The pg is divided into anterior and posterior lobes, and both of which consist of numerous long digitate lobules. The lobules at the base of the long digitate lobules of posterior lobe are greatly short; here, we named as “short lobules.” All the lobules vary in size, disposition, length, and shape. The anterior lobe and posterior lobes are connected by an anterior–posterior duct (apd). Two efferent salivary ducts (esd), derived from corresponding posterior lobes, fuse to form a short common duct which enters into the saliva syringe. The ag is composed of a greatly tortuous and folded accessory salivary tube, a gular gland (gg) constituting of several acini, and an accessory salivary duct (asd). The asd joins the esd at the place where the latter emergences. Constituents and arrangement of the salivary glands, the number and shape of the long digitate lobules in the anterior and posterior lobes, and the visibility of the apd were promising characters for the taxonomic and phylogenetic analysis of Cicadoidea. The variations of secretory granules in size, shape, and electron density in lobule cells of pg of Platypleura kaempferi probably indicating different materials are synthesized. The absence of the infoldings of basal plasma membrane in the basal area of the cells and the presence of electron-lucent vesicles in the cytoplasm of the gg cells of P. kaempferi might suggest that the secretions of gg are more watery.

Gross morphology and ultrastructure of salivary glands of the mute cicada Karenia caelatata Distant (Hemiptera: Cicadoidea)

Salivary glands of the cicada Karenia caelatata Distant were investigated using light microscopy and transmission electron microscopy. The salivary glands are paired structures and consist of principal glands and accessory glands. The principal gland is subdivided into anterior lobe and posterior lobe; the former contains about 34–39 long digitate lobules, while the latter contains approximately 30–33 long digitate lobules and 13–22 short digitate lobules. These short digitate lobules, about one fifth or sixth as long as the long digitate lobules, locate at the base of the long digitate lobules of posterior lobe. All of these digitate lobules vary in size, disposition, length and shape. The anterior lobe and the posterior lobe are connected by an anterior-posterior duct. Two efferent salivary ducts, which connect with the posterior lobe, fuse to form a common duct. The accessory gland is composed of three parts: a greatly tortuous and folded accessory salivary tube, a circlet of gular gland constituting of several acini of the same size, and a non-collapsible accessory salivary duct. The digitate lobules and gular glands possess secretory cells containing abundant secretory granules vary in size, shape, and electron density, as might indicate different materials are synthesized in different secretory regions. The anterior-posterior duct lines with a player of cuticular lining, and cells beneath the cuticular lining lack of basal infoldings, as suggests the duct serves just to transport secretions. The accessory salivary duct is lined with cuticular lining; cells of the duct have well developed basal infoldings associated with abundant mitochondria, as probably suggests the duct is a reabsorptive region of ions. The cells of the accessory salivary tube possess deep basal infoldings and well developed apical dense microvilli, indicating the cells of the tube are secretory in function. Concentric lamellar structures and a peculiar structure with abundant membrane-bound vesicles and secretory granules are observed for the first time, but their derivation and function remain unclear. The morphology and ultrastructure differences observed in the principal glands and accessory gland of the salivary glands of K. caelatata indicate that the sheath saliva was secreted by the principal glands, and the watery saliva was secreted by the accessory salivary glands. Rod-shaped microorganisms are found in the salivary glands (i.e., accessory salivary duct, gular gland, and long digitate lobule of salivary glands) for the first time, and their identity, function, and relationship to microorganisms residing in the salivary glands and/or other parts of alimentary canal of other cicadas need to be investigated further.

The interscale skin of the intermandibular‐gular regions of Alligator mississippiensis serves as a distribution system for the conditioning secretion of the gular gland

The skin of alligators is covered by plate‐like, non‐imbricate and hard‐cornified scales that are separated by a network of soft‐cornified interscale skin. The width of the interscale skin is correlated with the local expansibility of the skin. In most of the intermandibular‐gular region, the skin needs to stretch significantly when large prey items are swallowed to allow for the expansion of the pharynx. The interscale skin is widest along the mandibular rami where it forms longitudinal folds and channels that radiate rostrally from the paired gular gland orifices. The surface of these interscale channels is studded with small scale bumps. These wide channels are interconnected by a network of smaller, stretchable channels, whose surface structures are regionally distinct. The structured surface of the channels may enhance capillary action of the oily gular gland secretion as it is massaged through the channels by movements of the intermandibular‐gular skin during deglutition. This configuration of the intermandibular‐gular skin suggests that the channels serve to distribute the oily secretion of the gular gland to condition the stretchable interscale skin so as to keep it pliable and elastic. In contrast, the unyielding interscale skin in the area that subtends the hyoid and larynx is very narrow and has a smooth surface structure.

Histological examinations of facial glands in Saccopteryx bilineata (Chiroptera, Emballonuridae), and their potential use in territorial marking

Scent marking is widespread among individuals of Mammalia species, especially in resource defence social systems. Apart from urine and faeces that are used for claiming resource ownership, specialised scent glands are the main source of secretions in scent marking individuals. Most previous studies have described secretory epithelia macroscopically, since many glands are conspicuous. But macroscopically inconspicuous scent glands or morphological structures might then be overlooked. In Saccopteryx bilineata (greater sac-winged bat), behavioural observations suggest that both sexes have, apart from the conspicuous gular glands of males, specialised facial glands to display territorial marking. We investigated the facial glands of two males and one female S. bilineata histologically and found, first, that both sexes possess a bilateral symmetrically intermandibular gland, which is composed of a bed of modified apocrine sudoriferous cells. Second, we found lip glands consisting of modified apocrine sudoriferous cell units with pigmented ducts around the upper and the lower lip. Both gland types are probably involved during territorial marking.

First Record of the Genus Acanthixalus Laurent, 1944 from the Upper Guinean Rain Forest, West Africa, with the Description of a New Species

Abstract We describe a new species of Acanthixalus from southwestern Ivory Coast. Acanthixalus sonjae sp. nov. differs from the Central African Acanthixalus spinosus genetically by 4.6 % in the investigated 16S rRNA. Morphologically adult frogs are very similar to A. spinosus. Male A. sonjae have wider heads and probably smaller gular glands than A. spinosus. Tadpoles of A. sonjae differ by much longer tails. Acanthixalus sonjae males are apparently mute. The new species is semiaquatic and lives in large water-filled cavities of trees in secondary and primary rain forest. Tadpoles complete metamorphosis in three months. They are at least partly carnivorous.

Individual variation in perfume blending in male greater sac-winged bats

Male greater sac-winged bats, Saccopteryx bilineata, use hovering flights to court females in their harem territory. While hovering, males fan a fragrant perfume from sac-like organs in the wing membrane towards the females. Each afternoon, males renew the perfumes of their wing sacs during a stereotypical and time-consuming behavioural sequence, which includes blending secretions from genital and gular glands. I investigated whether male perfume-blending behaviour varies between the mating and the nonmating season, and whether successful males, those with large harems, have different patterns of perfume blending than less successful males. I measured variation in perfume-blending behaviour in 21 adult males. The pattern of perfume blending was not significantly different between the mating and the nonmating season. However, the time at which perfume blending began and terminated differed between seasons. During the mating season, males spent about the same time cleaning their wing sacs during phase I of perfume blending, irrespective of the number of females in their harem. During phase II, males with large harems spent significantly less time refilling and blending perfume than males with small harems. In addition, males with large harems took up fewer droplets of secretion from the genital region. Overall, male–male interactions were rare during perfume blending, and the decrease in duration in phase II was not attributable to more disturbance in large harems. There was also no evidence that males prevented each other from transferring secretions into their wing sacs. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Storage and display of odour by male Saccopteryx bilineata (Chiroptera, Emballonuridae)

Males of the sac-winged bat, Saccopteryx bilineata, actively fill their propatagial sacs with secretions from the genital region, the gular gland, urine and saliva. From our observations and those of Starck we deduce that propatagial sacs in S. bilineata do not have a glandular function, but are instead organs for the storage and display of odours. In addition to the already known “salting” and hovering behaviour of male S. bilineata, we describe in detail how odour is fanned to roosting individuals during the complex, stereotypic hovering displays. S. bilineata males also coat the fur of their backs with saliva using the wing tip and might scent-mark territory boundaries. “Yawning” may represent a visual as well as an olfactory cue. Odour seems to play an important role in the social communication of S. bilineata and in other emballonurids, as revealed by the broad distribution of wing sacs in this family. S. bilineata males display odour during energetically costly hovering flights in front of females. We demonstrate that the number of hovering displays increases with harem size. The mating effort of S. bilineata males comprises a multimodal signalling behaviour. Although males defend harem territories in which females gather, females seem to be able to choose the father of their progeny freely among the males of a colony. This may have led to the evolution of the complex mating displays by male S. bilineata.

Gular scent glands in adult female white-faced saki, Pithecia pithecia pithecia, and field observations on scent-marking behaviour.

Gular scent glands in adult female white-faced saki, Pithecia pithecia pithecia, and field observations on scent-marking behaviour.

Bacteria in the gular and paracloacal glands of the American alligator (Alligator mississippiensis; Reptila, Crocodilia)

All extant crocodilians possess two main exocrine skin glands: gular glands, located on the ventral surface of the lower jaw, and paracloacal glands, embedded in the walls of the cloaca. Twenty-three species of bacteria were isolated from the gular and the paracloacal gland secretions of the American alligator (Alligator mississippiensis). All but two of the bacteria genera indicated-Bacillus and Corynebacterium-were Gram-negative rods and cocci. Edwardsiella tarda and Escherichia coli were among the most common species indicated in both exudates. Citrobacter freundii, Enterobacter cloacae and other typically enteric organisms occur in one or both glands. No significant differences in the microbiota inhabiting the gular and the paracloacal were detected

Analysis of gular and paracloacal gland secretions of the american alligator (Alligator mississippiensis) by thin-layer chromatography Gland, sex, and individual differences in lipid components

Secretions from the gular and the paracloacal glands of adult male and female American alligators (Alligator mississippiensis) were extracted with chloroform, weighed, and analyzed by thin-layer chromatography. In both sexes, more lipoidal secretions were recovered from the paracloacal glands than from the gular glands. Females produce more lipoidal secretions in both sets of glands than do males. The thin-layer chromatograms of extracts from both glands exhibit bands consistent with aliphatic alcohols, sterols, free fatty acids, and steryl esters. Triglycerides, hydrocarbons, phosphatidylethanolamine, and lysophosphatidylcholine also are indicated in some chromatograms. Gland, sex, and individual differences are suggested in the thinlayer profiles.

The Gular Glands of Alligator mississippiensis: Histology and Preliminary Analysis of Lipoidal Secretions

The histology of the gular glands of adult Alligator mississippiensis and a preliminary analysis of gular gland secretions are described. The capsule of the gland consists of an outer layer of striated muscle and an inner layer of connective tissue. Septa lined with melanocytes radiate from the connective tissue layer of the capsule to the border of a central conglomerate of cells, cell fragments, and secretions. Parenchymal cells containing lipid droplets degenerate as they move toward the central region of the gland. The polar and nonpolar lipid fractions of gular gland secretions were separated and subjected to thinlayer chromatography with known lipid standards to allow tentative identification of the gland constituents. Bands consistent with sterols, free fatty acids, triglycerides, steryl esters, and ceramides are among those observed. A carbon13 nuclear magnetic resonance spectrum of whole gular gland secretions displays signals consistent with long-chain and esterified materials and provides additional evidence for some lipid classes indicated by thin-layer chromatography.

Notes: Lipids in the Gular Gland Secretion of the American Alligator (Alligator mississippiensis)

Lipids from the gular glands of the American alligator (Alligator mississippiensis) were examined by gas chromatography-mass spectroscopy. C14, C16, and C18 fatty acids, squalene, and α-tocopherol (vitamin E) were detected in nearly all samples. Cholesterol was detected clearly in several samples.

Gruczoł szyjny u nietoperza Taphozous longimanus

The morphology, histology and histochemistry of the gular gland of the Indian sheath-tailed bat, Taphozous longimanus Hardwicke, 1823, are described. A gular gland which is presented only in the male is a flattened, pear-shaped structure laying below the skin on the ventral side of neck.