The uropygial gland of the monk parakeet Myiopsitta monachus: Histology,morphogenesis, and evolution within Psittaciformes (Aves)

We describe the morphology, histology, and histochemical characteristics of the uropygial gland (UG) of the monk parakeet Myiopsitta monachus. The UG has a heart‐shape external appearance and adenomers extensively branched with a convoluted path, covered by a stratified epithelium formed by different cellular strata and divided into three zones (based on the epithelial height and lumen width), a cylindrical papilla with an internal structure of delicate type and two excretory pores surrounded by a feather tuft. Histochemical and lectin‐histochemical techniques performed showed positivity against PAS, AB pH 2.5, AB‐PAS, and some lectines, likely related to the granivorous feeding habits. Also, we describe the morphogenesis of the UG of the monk parakeet, which appears at embryological stage 34 as a pair of ectodermal invaginations. Heterochronic events in the onset development of the UG when compared with other birds could be recognized. Finally, to examine the phylogenetic occurrence of the UG within the Psittaciformes and infer its evolutionary history, we mapped its presence/absence over a molecular phylogeny. The reconstruction of the characters states at ancestral nodes revealed that the presence of the UG was the plesiomorphic feature for Psittaciformes and its loss evolved independently more than once.     

Recessive inherited doubling of the chicken's uropygial gland papilla

A new mutation that causes doubling of the uropygial gland (oil gland) papilla is described, and data that demonstrate its inherited basis are presented. This condition, which has been given the name "double oil gland papilla," varies in its expression: some individuals show only an indention of the papilla tip, while others exhibit a complete cleavage of the papilla such that two completely separate papillae project from a single oil gland. The data presented show that a single autosomal recessive gene, dgp, is the main determinant of this trait, but that its expression may also be influenced by background genetic factors as well as sex. Males more frequently are of the extreme doubling expression while females more frequently express the milder indented phenotype. Approximately 4% of mutant females are classified as normal. A linkage test with the rose comb gene showed independent segregation.     

The role of uropygial gland on sexual behavior in domestic chicken Gallus gallus domesticus

Recent studies have indicated that avian social behavior is influenced by olfactory cues. During the reproductive season a change in the chemical composition of uropygial gland secretion has been reported in some species and the hypothesis that olfactory signals may be produced by this gland has been proposed. To examine this hypothesis we performed two behavioral experiments to determine whether a female’s uropygial gland produce chemical signals that stimulate mating behaviors in domestic chickens. In Experiment 1 the role of the female’s uropygial gland in male mating behavior was examined by removing and examining the female’s uropygial gland. The frequency of mounts and copulations of intact male birds with sham-operated female birds was significantly higher than with uropygial glandectomized female birds. With respect to the number of waltzing that is one of the courtship displays intact males showed no significant difference between sham-operated female birds and uropygial glandectomized female birds. In Experiment 2 the relationship between male olfaction and the female’s uropygial gland was investigated using olfactory bulbectomized male birds. The number of mounts and copulations of sham-operated male birds with sham-operated female bird was significantly higher than with uropygial glandectomized female birds. In contrast olfactory bulbectomized male birds showed no significant differences in the number of mounts and copulations between sham-operated female birds and uropygial glandectomized female birds. These results indicate that intact and sham-operated male birds prefer to mate with female birds with the uropygial gland. The number of courtship waltzing of sham-operated male birds showed no significant difference. However olfactory bulbectomized male birds significantly courted to uropygial glandectomized female birds. Summarizing our results show that while anosmic males did not have any preference both intact and sham-operated male birds chose to mate with female birds having an intact uropygial gland suggesting that mate preference involves in male olfaction and that the female’s uropygial gland acts as a source of social odor cues in domestic chickens.     

Body‐mass‐dependent trade‐off between immune response and uropygial gland size in house sparrows Passer domesticus

Parasites greatly impact host fitness. The immune system is fundamental to combat endoparasites, and survival increases with greater investment in immunity. Some ectoparasites, by contrast, are reportedly combated by the use of the uropygial gland, an organ exclusive to birds, which secretes an oily substance (preen oil) that is spread on plumage. However, both mounting an immune response against a parasite and producing uropygial gland secretion depend on the same resources, a situation which may induce trade‐offs between the two antiparasitic functions. In this study, I experimentally test whether immune response is traded off against uropygial gland size in the house sparrow Passer domesticus. In the experiment, a group of sparrows were injected with an antigen (lipopolysaccharide, LPS), which stimulates the immune system, while the other group received a sham injection. The uropygial gland of LPS‐treated birds decreased significantly more than that of the control birds after treatment. Nevertheless, the effect of the treatment was limited to house sparrows with low body mass, suggesting that heavy house sparrows were able to produce an immune response while maintaining a relatively large uropygial gland. Given that uropygial gland size is strongly related to production of preen oil, these results suggest that preen oil production declines in birds in poor body condition when resources are preferentially diverted to other demanding functions, such as the immune system. Considering that the uropygial gland is involved in several fitness‐related processes in birds, the trade‐off between immune response and uropygial gland size may have important consequences for bird life histories.     

Adrenocortical influence on histokinetics and lipid components of uropygial gland of immature chick

Adrenocortical influence on uropygial gland of 10-day old male white leghorn chicken was assessed by suppressing glucocorticoid level with metyrapone and following corticosterone and deoxycorticosterone acetate (DOC) treatments (im), 100 micrograms each on alternate day for a period of 15 days. Metyrapone treatment resulted in significant atrophy of the uropygial gland with a severe regression of the glandular alveoli due to cytopycnosis, cellular disintegration and drastic cell loss. Concomitantly, there was a depletion of glandular lipid and its diester wax fraction. Corticosterone, administered simultaneously with metyrapone, counteracted severe adverse effects of the latter on the uropygial gland. In the normal chicken also corticosterone alone caused glandular hypertrophy with increased rate of cell renewal and cell growth within the alveoli and, to a lesser extent, augmented output of the glandular lipids. Simultaneous administration of corticosterone and testosterone propionate (TP), on the other hand, caused a moderate suppressive influence on this gland. DOC treatment alone or with metyrapone and TP failed to exert any noteworthy change in the uropygial gland excepting a moderate reduction of gland weight and a rise of glandular lipids observed after combined injections of DOC with TP and with metyrapone respectively.     

Glycan expression as a tool for a deeper understanding of a reproductive gland in a skate of economic importance

Atlantoraja platana is an oviparous skate endemic to the south-west Atlantic Ocean, and is one of the skate species most exploited by local industrial bottom trawl fisheries. Oviparous elasmobranchs encapsulate their eggs in complex egg cases produced by the oviductal gland (OG). This organ is exclusively present in these fishes and comprises four distinct zones: club, baffle, papillary and terminal. The relative size and structural complexity of these zones correlate with mode of reproduction. Glycans are known to play major roles in reproduction so their distribution in each zone of the OG could explain the functional multiplicity of the gland in skates, but this topic has not been previously investigated. In this study, morphological, histochemical and lectin-histochemical analysis revealed various novel aspects of A. platana's OG. The club, papillary and terminal zones positively stained for periodic acid Schiff's reagent (PAS) and Alcian Blue (AB), indicating the presence of neutral and acid mucopolysaccharides. However, the buffle zone was negative for PAS and AB stains, but was positive for all the lectins used. Each zone of the OG had a characteristic pattern of glycan expression. Finally, we confirmed the presence of sperm but not sperm storage. This is the first lectin-histochemical study of the OG in chondrichtyan fish and it has proven to be an important tool to understand some of the mechanisms of fertility and reproductive success in economic important species such as A. platana.     

Fine structure of the mandibular gland in pika (Ochotona rufescens rufescens)

The mandibular gland of the pika was examined by light microscopy, and transmission and scanning electron microscopies. The acinar cells were noted to be composed of serous cells and seromucous cells. The serous cells containing granules of moderate and high densities were slightly basophile and strongly positive to PAS, but were not stained with AB. The seromucous cells possessing less dense granules were light and moderately positive to PAS and AB. A sexual dimorphism was observed between these cells: Serous cells were considerably more frequent in males and seromucous cells were more numerous in females. Intercalated duct cells consisted of cuboidal light cells containing a few vesicles in the apical region. Striated ducts were comprised of two portions--a secretory portion and a typical striated portion without secretory granules. The secretory portion was composed of light and dark cells having secretory granules varying in size and density. The epithelium of typical striated portion consisted of light and dark cells containing fine vacuoles and vesicles.     

From preen secretions to plumage: the chemical trajectory of blue petrels' Halobaena caerulea social scent

Petrel seabirds heavily rely on their olfactory sense and are thus appropriate models for the study of avian chemical communication. The uropygial secretions of blue petrels Halobaena caerulea, for instance, have been shown to encapsulate elaborate sociochemical information including species, gender and identity. Yet, it is the plumage, and not preening secretions per se, which acts as the final substrate of avian scents. Importantly, the chemical relationship between secretions from the uropygial gland, located at the dorsal base of the tail, and plumage lipids has been considered in only a handful of studies which reported large qualitative differences. The emission process of avian scents, and the possible participation of the uropygial gland in particular, are therefore not elucidated. In the present study, we examine the early chemical trajectory of blue petrels' social chemosignals by comparing secretion and feather samples using Gas‐Chromatography Mass‐Spectrometry (GC/MS) and recently developed multivariate statistics. Our results indicate that (1) 85% of the feather lipids come from the uropygial secretions, (2) chemical differentiation between secretions and feather lipids includes qualitative and quantitative variations, which both have interesting implications for scent production, (3) the sociochemical information contained within the secretions (i.e. a sex‐specific signal and individual chemical signatures) are present in very conserved forms on the plumage. In the light of these results, it is apparent that the uropygial gland plays a critical role for chemical communication in petrels and possibly other avian groups.     

Histomorphological and histochemical characteristics of the intestine of the Senegal sole, Solea senegalensis.

The Senegal sole, Solea senegalensis has been exploited extensively in aquaculture from different countries; at present an intensive production of larvae and adults is being achieved with some nutritional problems. Since this species displays very different life styles and feeding habits at different stages of its life history (larvae, metamorphosis, adults), and because digestive mucins are implicated in different physiological processes including: increase of digestive efficiency, promotion of macromolecules-absorption, buffering of intestinal fluid, prevention of proteolytic damage to the epithelium and defence against bacteria, etc., we studied the histomorphological aspects, as well as the histochemical distribution of carbohydrates, (PAS, Alcian Blue), proteins (Bromophenol Blue), lipids (Oil Red O, Black Sudan B) and glycoproteins (Horseradish peroxidase-conjugated lectins) in the intestinal epithelium of adult Solea senegalensis specimens. Our data are compared with those obtained in larvae and adults of this and other fish species. Primary and secondary folds, microvilli of the intestinal enterocytes, as well as mucous or goblet cells were observed with a scanning electron microscope. Enterocytes and mucocytes of the intestine of adult Solea senegalensis were characterized by a rich supply of sugar and oligosaccharides. Carbohydrates (glycogen and mucins), proteins and lipids were present in cytoplasm and microvilli--brush border--of the enterocytes, which contain GalNAc, GlcNAc, Man, Glc and sialic acid-N-acetyl-D-galactosamine glycoconjugates. Intestinal mucous cells were strongly or weakly stained with Alcian Blue (pH 2.5 and 1). PAS reactivity was intense in numerous goblet cells, but some cells were PAS unreactive or weakly stained. Some goblet cells were positive for Bromophenol Blue but numerous cells were unstained; thus many proteins and possibly lipids may be conjugated with sugars. A similar reactivity to WGA and to neuraminidase-WGA was identified in some intestinal goblet, which were Con A unreactive, indicating the absence of Man and/or Glc and NANA glycoconjugates. GalNAc residues were only scarcely present in glycoproteins of some goblet cells.     

Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10-3, isolated from the uropygial gland of the hoopoe (Upupa epops)

The uropygial gland (preen gland) is a holocrine secretory gland situated at the base of the tail in birds which produces a hydrophobic fatty secretion. In certain birds, such as the hoopoe, Upupa epops, the composition of this secretion is influenced by both seasonal and sexual factors, becoming darker and more malodorous in females and in their nestlings during the nesting phase. The secretion is spread throughout the plumage when the bird preens itself, leaving its feathers flexible and waterproof. It is also thought to play a role in defending the bird against predators and parasites. We have isolated from the uropygial secretion of a nestling a bacterium that grows in monospecific culture which we have identified unambiguously by phenotypic and genotypic means as Enterococcus faecalis. The strain in question produces antibacterial substances that are active against all gram-positive bacteria assayed and also against some gram-negative strains. Its peptide nature identifies it as a bacteriocin within the group known as enterocins. Two peptides were purified to homogeneity (MR10A and MR10B), and matrix-assisted laser desorption ionization-time of flight (mass spectrometry) analysis showed masses of 5201.58 and 5207.7 Da, respectively. Amino acid sequencing of both peptides revealed high similarity with enterocin L50A and L50B (L. M. Cintas, P. Casaus, H. Holo, P. E. Hernández, I. F. Nes, and L. S. H?varstein, J. Bacteriol. 180:1988-1994, 1998). PCR amplification of total DNA from strain MRR10-3 with primers for the L50A/B structural genes and sequencing of the amplified fragment revealed almost identical sequences, except for a single conservative change in residue 38 (Glu-->Asp) in MR10A and two changes in residues 9 (Thr-->Ala) and 15 (Leu-->Phe) in MR10B. This is the first time that the production of bacteriocins by a bacterium isolated from the uropygial gland has been described. The production of these broad-spectrum antibacterial substances by an enterococcal strain living in the uropygial gland may be important to the hygiene of the nest and thus to the health of the eggs and chicks.     

Epidermal growth factor inhibits morphogenesis of the embryonic quail uropygial gland cultured in vitro

Formation of the uropygial papilla and glandular lumena was inhibited when the uropygial rudiment of a day 8 1/3 quail embryo was cultured for 2 days in a chemically defined medium in the presence of 50 ng/mL of epidermal growth factor (EGF). The epithelium of EGF-treated explants remained at the placode stage, or underwent minor invagination into the mesenchyme and became stratified like that of a 12- or 13-day-old embryo. EGF promoted cellular proliferation in the uropygial epithelium and the epidermis adjacent to the gland and it shortened the lag phase of proliferation and markedly stimulated epithelial DNA synthesis, detected immunocytochemically by labeling explants with 5-bromodeoxyuridine (BrdU). The maximal labeling index in EGF-treated uropygial epithelium was 55% higher than in the control. Electron microscopic observation revealed that the basal lamina had become irregular in the EGF-treated explants and that epithelial cytoplasmic processes penetrated through the basal lamina toward the mesenchyme. These same phenomena are observed in vivo when the glandular buds are formed during day 12–13. Some precocious changes occurred in the uropygial epithelium when the rudiment was cultured in the presence of EGF.     

Characterization of Antimicrobial Substances Produced by Enterococcus faecalis MRR 10-3, Isolated from the Uropygial Gland of the Hoopoe (Upupa epops)

The uropygial gland (preen gland) is a holocrine secretory gland situated at the base of the tail in birds which produces a hydrophobic fatty secretion. In certain birds, such as the hoopoe, Upupa epops, the composition of this secretion is influenced by both seasonal and sexual factors, becoming darker and more malodorous in females and in their nestlings during the nesting phase. The secretion is spread throughout the plumage when the bird preens itself, leaving its feathers flexible and waterproof. It is also thought to play a role in defending the bird against predators and parasites. We have isolated from the uropygial secretion of a nestling a bacterium that grows in monospecific culture which we have identified unambiguously by phenotypic and genotypic means as Enterococcus faecalis. The strain in question produces antibacterial substances that are active against all gram-positive bacteria assayed and also against some gram-negative strains. Its peptide nature identifies it as a bacteriocin within the group known as enterocins. Two peptides were purified to homogeneity (MR10A and MR10B), and matrix-assisted laser desorption ionization-time of flight (mass spectrometry) analysis showed masses of 5201.58 and 5207.7 Da, respectively. Amino acid sequencing of both peptides revealed high similarity with enterocin L50A and L50B (L. M. Cintas, P. Casaus, H. Holo, P. E. Hernández, I. F. Nes, and L. S. Håvarstein, J. Bacteriol. 180:1988-1994, 1998). PCR amplification of total DNA from strain MRR10-3 with primers for the L50A/B structural genes and sequencing of the amplified fragment revealed almost identical sequences, except for a single conservative change in residue 38 (Glu→Asp) in MR10A and two changes in residues 9 (Thr→Ala) and 15 (Leu→Phe) in MR10B. This is the first time that the production of bacteriocins by a bacterium isolated from the uropygial gland has been described. The production of these broad-spectrum antibacterial substances by an enterococcal strain living in the uropygial gland may be important to the hygiene of the nest and thus to the health of the eggs and chicks.     

Histochemical and immunohistochemical adaptations on the gastroesophageal tube of the blue-fronted parrot (Amazona aestiva Linnaeus, 1758)

Amazona aestiva Linnaeus, 1758 is known as the blue-fronted parrot. These animals are considered seed dispersion, contributing to ecological balance. Despite its ecological importance, A. aestiva is listed as an imminent danger of becoming extinct, as it is one of the most illegally traded native species in Brazil, besides losing its habitat due to deforestation and forest fires. The cranial oesophagus mucosa is lined with a non-keratinized stratified squamous epithelium, and the basal layer presents melanocyte accumulation. No mucous glands were observed in the lamina propria/submucosa. The ingluvium two different muscular layer patterns were observed, one internal and circular and one very thick, external and longitudinal. The proventriculum submucosa consists of polygonal proventricular glands and contents into a broad central duct lined with simple columnar epithelium Periodic acid-reactive Schiff positive (PAS+) and Alcian blue positive (AB+). The 5-HT cells are dispersed in the proventricular glands located at base and apex. The ventricle mucous layer contains numerous branched folds lined by a simple columnar epithelium. The epithelium was negative reaction for PAS and positive for AB only on the fold surfaces. The 5-HT cells were scarce and observed only at the base of the ventricular gland, as well as in the adjacent connective tissue.     

Ultrastructure of the acinar cells in the submandibular gland of the nine-banded armadillo

There are two discrete lobes comprising the armadillo subman-dibular gland. These two lobes can be defined grossly, histochemically and morphologically with the light and electron microscope. The minor lobe stains more intensely with PAS and AB. When viewed in the electron microscope, the secretory granules of the acinar cells within this lobe appear mucous-like. The granules of the demilune cells are slightly different in appearance. The secretory granules of the acinar cells in the major lobe contain many dense foci embedded in a fibrillar matrix, a substructure not described previously. The demilune cells of this lobe contain secretory granules with a mucous-like structure which is consistent throughout the entire lobe. As in the minor lobe, these demilune cells stain very intensely with PAS and AB.     

Uropygial gland size correlates with feather holes,body condition and wingbar size in the house sparrow Passer domesticus

The uropygial gland is an organ exclusive of birds that secretes an oily substance, the uropygial secretion, the functions of which are still debated. One of the proposed hypothesis is its possible action against chewing lice (order Phthiraptera), a group of avian ectoparasites that feed on feathers, causing different types of harm. However, this hypothesis lacks support. The present study analyses the relationship between uropygial gland size and the number of feather holes (which is correlated with the load of chewing lice) in the house sparrow Passer domesticus. Moreover, the relationship between the uropygial gland size and different aspects of sparrow health (body condition, immunocompetence and haematocrit), as well as sexually selected traits in males (badge and wingbar size), is tested. The results show a negative correlation between uropygial gland size and number of feather holes, a result found both years of the study. This result supports the hypothesis that uropygial secretion is used against chewing lice. Uropygial gland size also correlated positively with body condition (residuals of body mass relative to tarsus length) and immunocompetence, being therefore related to bird health. After a year in captivity, with resources provided ad libitum, no correlation was found between individual uropygial gland size and body condition or haematocrit, perhaps because the negative effect that chewing lice exert on bird health was offset by captivity conditions. Uropygial gland size was not correlated with badge size, but it was correlated with wingbar size, which furthermore supports the contention that this sexually selected signal acts as an indicator of lice resistance in the house sparrow. In summary, this study supports the idea of a positive relationship between uropygial gland and bird health in the house sparrow, the gland secretion affording resistance against chewing lice.     

Regeneration of acinar cells following ligation of rat submandibular gland retraces the embryonic-perinatal pathway of cytodifferentiation

Rat submandibular gland can regenerate following ligation-induced atrophy, eventually recovering its normal morphology and function. Previous studies have suggested that the regeneration process implies both self-proliferation of existing acini and formation of new acinar cells. One hypothesis is that new acinar cells may differentiate from the ductal cells in a similar fashion to the process of cytodifferentiation occurring during submandibular glandular development. In this study atrophy was induced, under recovery anaesthesia, by applying a metal clip on the main duct of the submandibular gland without including the chorda lingual nerve. After 2 weeks the duct was deligated for 3, 5 or 7 days or 8 weeks and the glands collected. Tissue was prepared for immunohistochemstry, biochemical analysis and RNA extraction. The histology of the regenerated glands shows several normal-looking acini, which have regained their glycoprotein content (AB/PAS positive), data also confirmed by biochemical analysis (SDS-PAGE/PAS). Regenerating tissue was characterized by the presence of embryonic-like branched structures ending with AB/PAS positive acinar cells. The proteins SMG-B and PSP are normally expressed in acinar cell precursors during development but only by intercalated ductal cells in the adult stage. In the adult regenerating gland mRNA levels of both SMG-B and PSP were found to be up-regulated compared to ligated glands and SMG-B expression localized to acinar cells whilst the ductal cells were negative. This study of rat submandibular gland regeneration suggests new acinar cells have differentiated from ducts and express markers of acinar cell precursors in a similar manner to the cytodifferentiation process occurring during glandular development.     

Seasonal variation in glycoconjugates of the pedal glandular system of the rayed Mediterranean limpet,Patella caerulea (Gastropoda: Patellidae)

Glycoconjugates secreted by the pedal system of the rayed limpet, Patella caerulea, were characterised in situ by histochemical and lectin-histochemical methods in individuals collected around the annual cycle, in November, March, and June. Stainings with periodic acid–Schiff (PAS), Alcian blue pH 2.5 (AB pH 2.5), Alcian blue pH 1.0 (AB pH 1.0), high-iron diamine–Alcian blue pH 2.5 and lectin binding assays with 9 lectins (Con A, WGA, succinylated-WGA, PNA, DBA, SBA, AAA, UEA-I, LTA) were performed. Four secreting cell types were observed in the sole, one in the peripheric region, and two in the sidewall. Glycoconjugate composition varied among cell types and also in one and the same cell type throughout the year. β-Elimination followed by PAS and AB pH 2.5 stainings indicated that most saccharidic chains were O-linked to the protein backbone. Secretion by sole and peripheric region was acidic, carboxylated and/or sulfated, whereas that of the sidewall was neutral. Glucosaminylated and 1,4-fucosylated residuals were predominant in the cell types along the year, 1,2-fucosylated residuals being observed only in the sidewall cells in June. Mannosylated and/or glycosylated residuals were observed in all cells mostly in November. Galactosylated/galactosaminylated residuals were present mostly in the sidewall cells and in the sole subepidermal mucocytes in June. Mannosylated and/or glycosylated residuals in November are probably linked to gonad maturation or to higher locomotion and foraging activity, whereas galactosaminylation in the sole cells and 1,2-fucosylation and glucosaminylation in the sidewall cells in June are linked to a prolonged stationary state, increasing water adsorption to counteract dehydration and/or to modulate microbial interactions.