Histological examinations of facial glands in <Emphasis Type="Italic">Saccopteryx</Emphasis><Emphasis Type="Italic">bilineata</Emphasis> (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.     

A histological study of cutaneous glands in the brown brocket deer

We examined the histological structure of 8 skin areas thought to contain cutaneous glands of potential importance in scent communication in 16 brown brocket deerMazama gouazoubira Fisher, 1814, using standard histological techniques. Frontal areas and preorbital sacs had scant glandular development. Sebaceous gland development was prominent in vestibular nasal glands and prepucial glands. Apocrine sudoriferous glands and sebaceous glands were well developed in tarsal glands, the caudal skin area and the interdigital glands of front and hind feet. The tail had a unique arrangement of apocrine sudoriferous glands. Anal glands had moderate glandular development, and metatarsal glands were absent. Several of these glandular areas may be important in the chemical communication among brocket deer.     

Lectin histochemical study on the infraorbital gland of the Japanese serow (Capricornis crispus)

Histology and lectin histochemistry were performed in the infraorbital gland of the Japanese serow. The gland is composed of glandular tissues and a pouch filled with the secretion. The tissues consist of an inner layer of sebaceous glands and an outer layer of apocrine glands. The male sebaceous layer is made up of the ordinary type, whereas the female's layer consists of the ordinary and modified types. In the apocrine gland stained with Arachis hypogaea (PNA), nine different patterns of glandular tubules were distinguished on the basis of staining of the cytoplasm, the Golgi area of secretory cells and secretion. Secretory modes of apocrine secretion and exocytosis were included in these stainings. Myoepithelial cells stained constantly with Glycine max (SBA) except when only the Golgi area of secretory cells was positive. The modified sebaceous gland was stained with PNA, SBA, Ricinus communis I (RCA), Triticum vulgaris (WGA), Canavalia ensiformis (Con A) and Ulex europaeus I (UEA), while the ordinary type was positive in PNA, RCA, SBA, WGA and Con A. The secretion in the pouch was stained with PNA, RCA, SBA, Dolichos biflorus (DBA), WGA and Con A. These findings suggest that the modified sebaceous gland contains large amounts of glycoconjugates and the apocrine gland shows a cyclic secretory process of apocrine secretion and exocytosis.     

Alpha 2u-globulin in modified sebaceous glands with pheromonal functions: localization of the protein and its mRNA in preputial, meibomian, and perianal glands

alpha 2u-Globulin, the principal urinary protein of the male rat, has extensive sequence homology with many lipid binding proteins. The highest concentration of alpha 2u-globulin is found in the preputial gland, a holocrine secretory organ with pheromonal function. Meibomian and perianal glands are two other modified sebaceous glands with holocrine secretory cycles and pleiomorphic peroxisomes capable of synthesizing pheromonal lipids. Immunocytochemical examination shows the presence of alpha 2u-globulin in the acinar cells of all three of these modified sebaceous glands. Whereas in the preputial gland all of the acinar cells exhibit immunoreactivity, in the meibomian and perianal glands only selective cells contain alpha 2u-globulin. In the case of the preputial gland, in addition to the acinar cells some stratified epithelial cells also were immunoreactive. In the perianal and meibomian glands, keratinocytes lining nearby hair shafts and select cells of accessory oil glands stained for alpha 2u-globulin. In situ hybridization with a cloned cRNA probe confirmed the immunocytochemical data. Presence of the alpha 2u-globulin mRNA in these glands was also established by Northern blot analysis. Immunoelectron microscopic examination of preputial alpha 2u-globulin showed the presence of this protein in secretory granules of various maturational stages. Immunolabeled alpha 2u was also found in attached vesicles containing protein and lipid inclusions. The lytic cells were not only loaded with alpha 2u-globulin but also contained sharp-edged, irregularly shaped electron-dense granules which stained heavily for this protein. Specific localization of alpha 2u-globulin and its mRNA in three pheromone-producing sebaceous glands and its structural homology with known lipid binding proteins indicate a pheromone carrier role of alpha 2u-globulin.     

The preputial gland of the Japanese serow Capricornis crispus: ultrastructure and lectin histochemistry

Preputial glands of the Japanese serow were found to consist of the modified sebaceous gland and apocrine gland in both sexes. In the modified sebaceous gland, cells transformed gradually toward the lumen from plentiful cytoplasm to a sponge-like network. Lipid droplets were observed in mitochondria of differentiating cells. By lectin histochemistry, differentiating cells were stained with Arachis hypogaea (PNA), Triticum vulgaris (WGA) and Canavalia ensiformis (Con A) lectins, while secretory cells of the apocrine gland revealed various stainings with PNA, Glycine max, Dolichos biflorus, WGA and Con A lectins. These findings suggest that glycoconjugates may have an active function in the preputial gland.     

Cultivation of epithelia from the secretory coil of the ovine apocrine gland: Evidence of secretory cell function and ductal morphogenesis In vitro

Summary The secretory coil of the ovine apocrine gland is composed predominantly of two cell types, secretory cells lining the lumen and myoepithelial cells adjacent to the basement membrane. The glands synthesize a number of hormones and growth factors, but analysis of the functions of these molecules may be hampered by the mixing of apocrine and sebaceous secretions in the pilary canal. The purpose of this study was to isolate the glands and devise simple culture procedures to facilitate investigations of secretory cell function. The most successful approach involved microdissection of the secretory coils individually from skin biopsies and culture in Dulbecco’s modified Eagle’s medium. After 1–2 wk in medium, cell outgrowths were seen from explants. These consisted predominantly of populations of epithelial cells, many containing granules. Smaller granules were usually concentrated around the cell nuclei and accumulated lipophilic dyes. Large granules were unreactive. Western analysis showed that cells in culture synthesized nerve growth factor-like peptides, a feature consistent with one of the functions of the gland in vivo. When isolated secretory coils were explanted to culture dishes coated with matrigel, highly compact, multilayered masses of cells grew out. Subsequently, tubular structures formed. The observations suggest that some differentiated functions of gland cells were retained in vitro and that the procedures described provide a system for the study of apocrine secretions in isolation from those of other skin glands.     

Cutaneous glands of male and female impalas (Aepyceros melampus): seasonal activity changes and secretory mechanisms

The cutaneous glands of the forehead and the metatarsus were studied by histological and histochemical methods and electron microscopy in adult male and female impalas in various seasons of the year. All glandular areas consist of apocrine and holocrine glands, which, however, occur in different proportions. Our findings in the apocrine gland cells suggest (1) the synthesis and exocytosis of a glycoproteinaceous secretory product stored in secretory granules, (2) typical apocrine secretion of the transformed apical cytoplasm, and (3) transepithelial fluid transport. The Golgi apparatus and apical membrane have binding sites for several lectins (PNA, HPA, RCA I, WGA). Cytokeratins 7, 14 and 19 are expressed at various intracellular localizations, suggesting an active role in the secretory mechanisms. The glands of the male forehead show marked seasonal changes in activity that are correlated with the main phases of the reproductive cycle, with the highest cellular activity occurring during the rut in April/May. The female forehead glands are only moderately developed and do not undergo seasonal changes. The metatarsal glands are of equal size in males and females and show no seasonal changes in activity. This study supports the hypothesis that (1) forehead glands in the male have a signaling role in the rut and (2) the metatarsal glands have a more general, probably social role maintaining and restoring contact between herd members.     

Steroid regulation of territorial scent marking in the Mongolian gerbil (Meriones unguiculatus)

Mongolian gerbils (Meriones unguiculatus) display a territorial scent marking response associated with a ventral sebaceous gland. In males, both the gland and behavior are androgen dependent and hormone control of marking is delimited to the preoptic area. The present study examines the effects of eleven steroids, injected subcutaneously or implanted into the preoptic area, on territorial marking in adult male castrates. Steroid effects on ventral gland function are also described. The neural target cells that mediate marking respond to a narrower range of steroids than do peripheral target cells in the ventral gland. Testosterone appears to be the only endogenous steroid capable of eliciting marking in males. Other steroids which share molecular commonalities with testosterone (a 17β-hydroxyl group and a double bond involving carbon 4) also induce marking behavior. Central receptors may recognize the relevant endogenous steroid, testosterone, by these features.     

Testis-testicular gland complex of two Tripterygion species (Blennioidei, Teleostei): differences between territorial and non-territorial males

The morphological differences between the testis and testicular gland of territorial and nonterritorial males of Tripterygion tripteronotus and T. delaisi were examined and correlated with differences in reproductive behaviour. In territorial males of both species the testicular gland is much more developed than in non-territorial males. Larger cellular and nuclear sizes in the territorial males indicate that the activity of the gland cells is enhanced. These cells contain SER, numerous lipid droplets and mitochondria with lamellar cristae. Absence of 3β-HSD activity at these sites points to lack of a steroidogenic potency. In both territorial and non-territorial fish, steroid-producing Leydig cells have been demonstrated in the connective tissue betweeen the testis and the testicular gland, and around the collecting sperm duct. In addition, 3β-HSD activity has been found in the scarce interstitial Leydig cells of territorial fish. Morphometric data indicate an enhanced activity of the Leydig cells in territorial fish.     

Localization of gamma-glutamyl transpeptidase in human sweat glands: an immunohistochemical study using a monoclonal antibody

We studied the distribution of gamma-glutamyl transpeptidase (gamma-GT) by use of a monoclonal antibody (MAb) against human kidney gamma-GT in human sweat glands. In the eccrine sweat gland, the enzyme was localized along the luminal membrane and small apocrine extrusions of the superficial cells of the secretory portion. The intercellular canaliculi between basal cells were occasionally immunoreactive. In the secretory portion of the apocrine gland, luminal membrane and apocrine extrusions of various sizes and stages at the apices of the secretory cells exhibited positive reactions. Immunoreaction was also seen in the Golgi area of the cuboidal secretory cells. No positive reaction was observed in the myoepithelial cells of either gland or in the excretory duct cells.     

Specialized mucous glands and their possible adaptive role in the males of some species of Rana (Amphibia,Anura)

A structural and ultrastructural study was carried out on the cutaneous glands in some species of Rana (R. dalmatina, R. iberica, R. italica, R. "esculenta," and R. perezi), giving particular attention to the mucous secretory units. Two different types of mucous glands occur in R. dalmatina, R. iberica, and R. italica. Besides the ordinary mucous units, which are randomly distributed over the body surface in both males and females, a further population of mucous glands was observed on the male dorsal skin. The latter is recognizable by the peculiar morphology of the epithelial cells and some characteristics of the secretory product. Specialized mucous glands are absent in both sexes of R. "esculenta" and R. perezi. The possible adaptive role of the specialized mucous glands is discussed in light of the absence of vocal sacs in males of R. dalmatina, R. iberica, and R. italica. Chemosignals released by sexually dimorphic mucous units may replace vocal communication during the breeding season and so play an important role in female attraction and/or territorial announcement. The morphology and possible function of the specialized mucous glands in the three species of Rana are compared with the breeding glands of other frogs and with the hedonic glands of some urodeles (Salamandridae and Plethodontidae), which are known to produce pheromonal substances during courtship.     

Evolutionary origins of the mammary gland

Because the mammary gland has no known homologue among the extant reptiles, attempts to reconstruct its evolution must focus on evidence from living mammals. Of the numerous structures that have been hypothesized to have given rise to the mammary gland, only three remain as plausible progenitors: sebaceous glands, eccrine glands and apocrine glands. Ancestral mammary glands are usually assumed to have produced a copious watery secretion like that of human eccrine sweat glands. However, in terms of anatomy, physiology, development and topographical distribution, mammary glands are more similar to apocrine and sebaceous glands than to typical eccrine glands. Nevertheless, each of the three populations of cutaneous glands exhibit specializations unlikely to be primitive for the mammary gland. The mammary gland either predated full differentiation of mammalian cutaneous glands or, more probably, evolved as a neomorphic mosaic that combined the properties of apocrine and sebaceous glands. Consequently, ancestral, prototypic lacteal glands may have had the capacity to synthesize and secrete small amounts of organic substances, as do sebaceous and apocrine glands of living mammals.     

Scent marking in a territorial African antelope: I. The maintenance of borders between male oribi

Scent marking is ubiquitous among the dwarf antelope and gazelles of Africa, but its function has been the subject of debate. This study examined preorbital gland scent marking in the oribi, Ourebia ourebi, a territorial African antelope. Several hypotheses for the function of scent marking by territorial antelope were tested with observational data. Of these, the hypotheses that scent marking is driven by intrasexual competition between neighbouring males, and that marks serve as an honest advertisement of a male's ability to defend his territory from rivals, were supported best. Thirty-three territorial male oribi on 23 territories marked most at borders shared with other territorial males, and territorial males marked more often at borders shared with multimale groups than at borders shared with a single male. This suggests that males perceived neighbouring male groups as a greater threat to territory ownership than neighbouring males that defended their territories without the aid of adult subordinates. Marking rate was unrelated to territory size or the number of females on adjacent territories, but males with many male neighbours marked at higher rates than those with fewer male neighbours. These results suggest that the presence of male neighbours has a greater effect on the scent marking behaviour of territorial antelope than has been considered previously. Copyright 1999 The Association for the Study of Animal Behaviour.     

Structure of the inguinal gland in the mountain hare in various states of reproductive activity. I. The sebaceous glands

Histology and ultrastructure of sebaceous glands of the integumental inguinal gland of the hare were studied during the periods of low and high reproductive activity (in winter and in spring breeding season). It was established that the glands were functioning continually (cells in acini of all the animals used contained numerous secretory granules). The expansion of agranular endoplasmic reticulum and Golgi complex in secretory cells of sexually active animals, especially of males, shows an increased intensity of gland secretory process during the breeding season.     

The skin of primates. XXXVI. The skin of the pigmy marmoset--Callithrix (Cebuella) pygmae

The pigmy marmoset — Callithrix (= Cebuella) pygmaea Spix — is the second detailed study of the members of the family Callithricidae. It is closely allied to the red-mantled tamarin — Saguinus (=Tamarinus) fuscicollis illigeri Spix — and shares some of its characteristics with both Prosimii and Anthropoidea. The epidermis and dermis contain moderate numbers of concurrent, melanotic melanocytes. The dermis is rich in elastin. Hair follicles grow in groups of three or four over the general body surface, and one apocrine gland is associated with each grouping. Arrectores pilorum muscles are well developed. On the ventral ulnar wrist are sinus hairs associated with apocrine glands. Most hair follicles have nerve end-organs around them that are reactive for acetylcholinesterase and alkaline phosphatase. There is a large aggregation of sebaceous glands in the suprapubic region. The large sebaceous glands in the eyelid, face, and external genitalia are surrounded by cholinesterasereactive nerves. Apocrine glands are found over most of the hairy skin except the brow, scalp and back; a large grouping of them is present in the sternal region. Only the secretory coils of apocrine glands in the external genitalia are invested with butyrylcholinesterase-rich nerves. Eccrine glands are confined to the volar surfaces of the pes and manus. They have dark cells with abundant glycogen and clear cells with neither glycogen nor PAS-reactive material. The nerves around the eccrine secretory coil are reactive only for acetylcholinesterase.     

Jugulo-sternal-gland tumors in male tree shrews (Tupaia belangeri).

Adenocarcinomas of the jugulo-sternal glands were observed in seven adult male tree shrews (Tupaia belangeri) at biopsy or necrospy. Five of these tumors were classified as carcinomas of the sebaceous gland compartment; one was diagnosed as a papilliform adenoma of apocrine (monoptychic) sweat glands; and one was of a mixed sebaceous gland/apocrine sweat gland structure. Four sebaceous gland carcinomas had histologic evidence of vascular invasion; one had metastasized to the regional lymph nodes and lungs and had also invaded the thoracic muscles.     

The frontal and gular dermal scent organs of the marsupial sugar glider (Petaurus breviceps)

A study spanning two breeding seasons was carried out to examine the role of androgens in the control of the frontal and gular scent glands of the marsupial sugar glider Petaurus breviceps Waterhouse in a wild population. Animals were captured at monthly intervals and from these blood samples were taken and tissue biopsy samples were collected from the scent glands.
Several histological parameters underwent seasonal changes which were related to changes in the plasma concentration of free plus albumin bound ('biologically active') testosterone. The parameters which showed significant change did so during the July-September breeding season coinciding with the peak in biologically active testosterone concentration.
Castration caused a significant decrease in the nuclear diameters of gular and frontal apocrine and sebaceous gland cells, and a decrease in gular apocrine cell height. These decreases were reversed with androgen replacement therapy.
The nuclear diameters of apocrine tissue cells in both scent organs are positively correlated with the plasma level of biologically active testosterone. In the gular organ, but not in the frontal organ, the depth of apocrine tissue was significantly correlated with nuclear diameter. In castration and androgen replacement studies gular apocrine tissue responded more dramatically than did frontal apocrine tissue. This suggests that the gular organ is more sensitive to testosterone than is the frontal.     

Sexual differences and effects of castration on secretory mode and intracellular calcium ion dynamics of golden hamster Harderian gland

The aim of the present work was to study the sexual differences in secretory mechanisms and intracellular calcium ion dynamics in the Harderian gland of the golden hamster. In both sexes the Harderian gland consisted of small and large lobes. In the intact control male glands the secretory portions of both lobes showed wide lumina that contained secretory material and cytoplasmic fragments, suggestive of the occurrence of exocytosis and apocrine secretion. After perfusion with HEPES-buffered Ringer's solution containing 10 microM carbamylcholine (CCh), the glandular cells showed features of enhanced secretion and a rise in intracellular calcium concentration ([Ca2+]i). In the intact control female gland the lumina of most secretory portions in the large lobe contained porphyrin accretions, and exocytosis was the sole secretory mechanism. Stimulation of the large lobe with 10 microM CCh did not raise [Ca2+]i or cause enhanced secretion. The small lobe in females resembled the male gland in secretory functions, and CCh administration caused enhanced secretion and a rise in [Ca2+]i. Castration in males abolished apocrine secretion; exocytosis became the sole secretory mechanism, and stimulation of the glandular cells with CCh did not cause enhanced secretion or induce a rise in [Ca2+]i. To the contrary, in females, castration restored apocrine secretion and CCh administration caused enhanced secretion and a rise in [Ca2+]i. Castration did not affect the secretory mechanisms and the effect of CCh on the glandular cells in the small lobes of both male and female glands. The present study points to the possibility that sex hormones may control the functioning or expression of muscarinic receptors in the Harderian gland of the golden hamster.     

Fishy Aroma of Social Status: Urinary Chemo-Signalling of Territoriality in Male Fathead Minnows (Pimephales promelas)

Chemical structures of several urinary reproductive pheromones in fish have been identified, and their role in the chemical communication of reproductive condition is well characterized. On the contrary, the role of chemical communication in signalling of social/territorial status in fish is poorly understood. Fathead minnows are an example of a fish species whose life history traits appear conducive to evolution of chemical communication systems that confer information about social/territorial status. Male reproduction in this species is dependent upon their ability to acquire and defend a high quality nesting territory, and to attract a female to the nest. We hypothesized that fathead minnow males use visual and urine-derived chemical cues to signal territorial status. To test this hypothesis, effects of territorial acquisition on male-specific secondary sex characteristics (SSCs) and urine volumes were first assessed. Second, frequencies of male urination in varying social contexts were examined. Finally, nuclear magnetic resonance-based metabolomics was used to identify urinary metabolites that were differentially excreted in the urine of territorial versus non-territorial males. The expression of SSCs, sperm, and urine volumes increased with territory acquisition, and either remained unchanged or decreased in non-territorial males. Frequency of male urination increased significantly in the presence of females (but not males), suggesting that females are the main target of the urinary signals. Territorial and non-territorial males had distinct urinary metabolomic profiles. An unforeseen finding was that one could discern future territorial status of males, based on their initial metabolomic profiles. Bile acids and volatile amines were identified as potential chemical signals of social status in the fathead minnow. The finding that trimethylamine (a fishy smelling volatile amine) may be a social cue is particularly interesting, because it is known to bind trace amine-associated receptors, indicating that these receptors may play role in chemical signalling of social status in fish.     

The histological and histochemical characteristics of the hepatoid circumanal glands in the dog: the features of similarity and difference with the skin glands of other types

Three types of skin glands, the derivatives of the outer root sheath of the hair follicle, have been compared, which are represented by hepatoid, sebaceous and apocrine sweat glands. There are three characteristic properties inherent to hepatoid glands, existence of a network of intercellular secretory tubules, lysis of some secretory cells during the duct formation which is not the fatty transformation and cyst formation.