Histological and histochemical study of the uropygial gland of chimango caracara (Milvago chimango vieillot, 1816)

The uropygial glands of birds are sebaceous organs that contribute to the water-repellent properties of the feather coat. We studied the histological and histochemical characteristics of the uropygial gland of chimango caracara using hematoxylin and eosin (H & E), Gomori´s trichrome, orcein, Gomori´s reticulin, periodic acid-Schiff (PAS), Alcian blue (AB) and a variety of lectins. The gland is composed of two lobes and a papilla with 20 downy feathers. It is surrounded by a capsule of dense connective tissue that contains elastic, reticular and smooth muscle fibers. The papilla is delicate and has two excretory ducts. The gland mass relative to body mass was 0.143%. Both adenomer cells and their secretions were stained with Sudan IV, PAS and AB, and were positive for numerous lectins that indicated the presence of lipids and carbohydrates. Immunohistochemical techniques to detect PCNA confirmed cell proliferation in the basal stratum of the adenomer cells. The lipids and glycoconjugates secreted by the uropygial gland serve numerous functions including protection against microorganisms.     

The Hoopoe's Uropygial Gland Hosts a Bacterial Community Influenced by the Living Conditions of the Bird

Molecular methods have revealed that symbiotic systems involving bacteria are mostly based on whole bacterial communities. Bacterial diversity in hoopoe uropygial gland secretion is known to be mainly composed of certain strains of enterococci, but this conclusion is based solely on culture-dependent techniques. This study, by using culture-independent techniques (based on the 16S rDNA and the ribosomal intergenic spacer region) shows that the bacterial community in the uropygial gland secretion is more complex than previously thought and its composition is affected by the living conditions of the bird. Besides the known enterococci, the uropygial gland hosts other facultative anaerobic species and several obligated anaerobic species (mostly clostridia). The bacterial assemblage of this community was largely invariable among study individuals, although differences were detected between captive and wild female hoopoes, with some strains showing significantly higher prevalence in wild birds. These results alter previous views on the hoopoe-bacteria symbiosis and open a new window to further explore this system, delving into the possible sources of symbiotic bacteria (e.g. nest environments, digestive tract, winter quarters) or the possible functions of different bacterial groups in different contexts of parasitism or predation of their hoopoe host.     

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.     

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.     

Exploring the adjustment to parasite pressure hypothesis: differences in uropygial gland volume and haemosporidian infection in palearctic and neotropical birds

Parasites are globally widespread pathogenic organisms, which impose important selective forces upon their hosts. Thus, in accordance with the Adjustment to parasite pressure hypothesis, it is expected that defenses among hosts vary relative to the selective pressure imposed by parasites. According to the latitudinal gradient in diversity, species richness and abundance of parasites peak near the equator. The uropygial gland is an important defensive exocrine gland against pathogens in birds. Size of the uropygial gland has been proposed to vary among species of birds because of divergent selection by pathogens on their hosts. Therefore, we should expect that bird species from the tropics should have relatively larger uropygial glands for their body size than species from higher latitudes. However, this hypothesis has not yet been explored. Here, we analyze the size of the uropygial gland of 1719 individual birds belonging to 36 bird species from 3 Neotropical (Peru) and 3 temperate areas (Spain). Relative uropygial gland volume was 12.52% larger in bird species from the tropics than from temperate areas. This finding is consistent with the relative size of this defensive organ being driven by selective pressures imposed by parasites. We also explored the potential role of this gland as a means of avoiding haemosporidian infection, showing that species with large uropygial glands for their body size tend to have lower mean prevalence of haemosporidian infection, regardless of their geographical origin. This result provides additional support for the assumption that secretions from the uropygial gland reduce the likelihood of becoming infected with haemosporidians.     

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.     

Ectoparasites, uropygial glands and hatching success in birds

The uropygial gland of birds secretes wax that is applied to the plumage, where the secretions are hypothesized to eliminate fungi and bacteria, thereby potentially providing important benefits in terms of plumage maintenance. We analyzed variation in size of the uropygial gland in 212 species of birds to determine the function and the ecological correlates of variation in gland size. Bird species with larger uropygial glands had more genera of chewing lice of the sub-order Amblycera, but not of the sub-order Ischnocera, and more feather mites. There was a fitness advantage associated with relatively large uropygial glands because such species had higher hatching success. These findings are consistent with the hypothesis that the uropygial gland functions to manage the community of microorganisms, and that certain taxa of chewing lice have diverged as a consequence of these defenses.     

Synthesis of multimethyl-branched fatty acids by avian and mammalian fatty acid synthetase and its regulation by malonyl-CoA decarboxylase in the uropygial gland

Fatty acid synthetase, partially purified by gel filtration with Sepharose 4B from goose liver, showed the same relative rate of incorporation of methylmalonyl-CoA (compared to malonyl-CoA) as that observed with the purified fatty acid synthetase from the uropygial gland. In the presence of acetyl-CoA, methylmalonyl-CoA was incorporated mainly into 2,4,6,8-tetramethyldecanoic acid and 2,4,6,8,10-pentamethyl-dodecanoic acid by the enzyme from both sources. Methylmalonyl-CoA was a competitive inhibitor with respect to malonyl-CoA for the enzyme from the gland just as previously observed for fatty acid synthetase from other animals. Furthermore, rabbit antiserum prepared against the gland enzyme cross-reacted with the liver enzyme, and Ouchterlony double-diffusion analyses showed complete fusion of the immunoprecipitant lines. The antiserum inhibited both the synthesis of n-fatty acids and branched fatty acids catalyzed by the synthetase from both liver and the uropygial gland. These results suggest that the synthetases from the two tissues are identical and that branched and n-fatty acids are synthesized by the same enzyme. Immunological examination of the 105,000g supernatant prepared from a variety of organs from the goose showed that only the uropygial gland contained a protein which cross-reacted with the antiserum prepared against malonyl-CoA decarboxylase purified from the gland. Thus, it is concluded that the reason for the synthesis of multimethyl-branched fatty acids by the fatty acid synthetase in the gland is that in this organ the tissue-specific and substrate-specific decarboxylase makes only methylmalonyl-CoA available to the synthetase. Fatty acid synthetase, partially purified from the mammary gland and the liver of rats, also catalyzed incorporation of [methyl-¹⁴C]methylmalonyl-CoA into 2,4,6,8-tetramethyldecanoic acid and 2,4,6,8-tetramethylundecanoic acid with acetyl-CoA and propionyl-CoA, respectively, as the primers. Evidence is also presented that fatty acids containing straight and branched regions can be generated by the fatty acid synthetase from the rat and goose, from methylmalonyl-CoA in the presence of malonyl-CoA or other precursors of n-fatty acids. These results provide support for the hypothesis that, under the pathological conditions which result in accumulation of methylmalonyl-CoA, abnormal branched acids can be generated by the fatty acid synthetase.     

Ultrastructural changes in the uropygial gland of the male Japanese quail,Coturnix coturnix,after testosterone treatment

Summary The ultrastructure of the uropygial gland of the male quail was compared to that of the sebaceous gland of the male rat after castration and testosterone treatment of both species. In intact animals, the differentiating cells of these glands displayed almost the same pattern as regards their smooth endoplasmic reticulum, an organelle involved in lipogenesis in both cases. Castration reduced the volume of this organelle, while testosterone administration restored cell morphology to a normal or supranormal level. Finally, this study showed that at ultrastructural level, there is a close functional analogy between the uropygial gland of quail and the sebaceous glands of rats as regards their androgen dependency. Consequently, the uropygial gland might be an attractive model for study of action of androgens on sebaceous-like glands.     

Chemotaxonomy of Anseriformes

The composition of the uropygial gland wax of 8 species of birds of the order Anseriformes was investigated. As was expected, the waxes are composed of more or less methyl-branched fatty acids and alcohols. The results obtained have been compared with those on other species of Anseriformes and discussed from a chemotaxonomical viewpoint. For this purpose the various parameters have been depicted on a 3-dimensional matrix.     

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.     

Preen oil and bird fitness: a critical review of the evidence

The uropygial gland is a holocrine complex exclusive to birds that produces an oleaginous secretion (preen oil) whose function is still debated. Herein, I examine critically the evidence for the many hypotheses of potential functions of this gland. The main conclusion is that our understanding of this gland is still in its infancy. Even for functions that are considered valid by most researchers, real evidence is scarce. Although it seems clear that preen oil contributes to plumage maintenance, we do not know whether this is due to a role in reducing mechanical abrasion or in reducing feather degradation by keratinophilic organisms. Evidence for a function against pathogenic bacteria is mixed, as preen oil has been demonstrated to act against bacteria in vitro, but not in vivo. Nor is it clear whether preen oil can combat pathogenic bacteria on eggshells to improve hatching success. Studies on the effect of preen oil against dermatophytes are very scarce and there is no evidence of a function against chewing lice. It seems clear, however, that preen oil improves waterproofing, but it is unclear whether this acts by creating a hydrophobic layer or simply by improving plumage structure. Several hypotheses proposed for the function of preen oil have been poorly studied, such as reduction of drag in flight. Similarly, we do not know whether preen oil functions as repellent against predators or parasites, makes birds unpalatable, or functions to camouflage birds with ambient odours. On the other hand, a growing body of work shows the important implications of volatiles in preen oil with regard to social communication in birds. Moreover, preen oil clearly alters plumage colouration. Finally, studies examining the impact of preen oil on fitness are lacking, and the costs or limitations of preen‐oil production also remain poorly known. The uropygial gland appears to have several non‐mutually exclusive functions in birds, and thus is likely to be subject to several selective pressures. Therefore, future studies should consider how the inevitable trade‐offs among different functions drive the evolution of uropygial gland secretions.     

The evolution of size of the uropygial gland: mutualistic feather mites and uropygial secretion reduce bacterial loads of eggshells and hatching failures of European birds

Potentially, pathogenic bacteria are one of the main infective agents against which a battery of chemical and physical barriers has evolved in animals. Among these are the secretions by the exocrine uropygial gland in birds. The antimicrobial properties of uropygial secretions may prevent colonization and growth of microorganisms on feathers, skin and eggshells. However, uropygial gland secretions also favour the proliferation of feather mites that feed on secretions and microorganisms living on feathers that would otherwise reach eggshells during incubation if not consumed by feather mites. Therefore, at the interspecific level, uropygial gland size (as an index of volume of uropygial secretion) should be positively related to eggshell bacterial load (i.e. the risk of egg infection), whereas eggshell bacterial loads may be negatively related to abundance of feather mites eating bacteria. Here, we explore these previously untested predictions in a comparative framework using information on eggshell bacterial loads, uropygial gland size, diversity and abundance of feather mites and hatching success of 22 species of birds. The size of the uropygial gland was positively related to eggshell bacterial loads (mesophilic bacteria and Enterobacteriaceae), and bird species with higher diversity and abundance of feather mites harboured lower bacterial density on their eggshells (Enterococcus and Staphylococcus), in accordance with the hypothesis. Importantly, eggshell bacterial loads of mesophilic bacteria, Enterococcus and Enterobacteriaceae were negatively associated with hatching success, allowing us to interpret these interspecific relationships in a functional scenario, where both uropygial glands and mutualistic feather mites independently reduce the negative effects of pathogenic bacteria on avian fitness.     

Diesters of 3-hydroxy fatty acids produced by the uropygial glands of female mallards uniquely during the mating season

The uropygial gland secretions produced by female mallards (Anas platyrhynchos) throughout the year were analyzed by thin-layer chromatography and combined gas-liquid chromatography and mass spectrometry. Most of the year, the secretion was composed of wax esters. With the beginning of the mating season in the middle of March, a polar component appeared which became the dominant and sole component of the secretion through April and May and as the mating season ended in June, wax esters became the sole component of the secretion. The polar components were identified to be diesters of n-C8, n-C10, and n-C12 3-hydroxy acids with n-C16 and n-C18 alcohols and n-C6 to C16 even chain acids. Immediately after the diester-producing period the female uropygial glands produced very long chain wax esters composed of fatty acids longer than C12. By the end of August, shorter chain wax esters composed of C6 and C12 acids became the dominant components of the secretion and this composition, previously considered characteristic of mallards, remained constant until March. The observed disappearance of the short chain waxes during the postnuptial period is similar to that in males. The dramatic changes in the composition of the uropygial glands similar to those observed in the female mallards during the mating season have not yet been observed in any other species.     

Histological remarks of the oviduct and the oviducal gland of Sympterygia acuta Garman, 1877

The elasmobranchs constitute an important resource in Argentinian fishing and they show reproductive characteristics that make them susceptible to the pressure of fishing. In spite of the importance of the resource our knowledge about the species of the Southwestern Atlantic is scarce. In this work we study the microanatomy of the oviduct and the oviducal gland of Sympterygia acuta. The results show a very folded oviduct with mucous and ciliated cells. The oviducal gland depicts the same zonation as other batoids, showing the typical four regions (club, papillary, baffle and terminal). The epithelium lining the glandular lumen is simple columnar with ciliated and glandular cells. The four zones show simple or ramified tubular gland the secretions of which constitute the egg's envelopes. The club and baffle zones are similar to those present in other species. The papillary one depicts a different pattern of secretions that other Rajiformes and the last zone of the gland is characterized by mixed adenomers. The information here exposed constitutes the first report on the microanatomy of the genital tract of S. acuta.     

Nestedness of hoopoes' bacterial communities: symbionts from the uropygial gland to the eggshell

How microbial symbionts are established and maintain on their hosts is a leading question with important consequences for the understanding of the evolution and functioning of mutualistic relationships. The acquisition by hosts of mutualistic microbial symbionts can be considered as colonization processes of environments (i.e., host) by symbionts. Colonization processes can be explored by characterizing the nestedness of communities, but this approach has rarely been applied to communities of microbial symbionts. We used this approach here, and estimated the nestedness of bacterial communities of hoopoes (Upupa epops), a species with symbiotic bacteria in their uropygial gland that are expected to colonize eggshells where they protect embryos from pathogens. Bacterial communities were characterized by ARISA (Automated rRNA Intergenetic Spacer Region) and studied the nestedness characteristics of bacterial communities living in the uropygial secretion, bill, belly and eggshells of each sampled female hoopoes. We detected a consistent nested pattern of bacterial communities of hoopoes; from the uropygial gland to the eggshell. We also found evidence of study year and reproductive events influencing the level of nestedness of bacterial communities of hoopoes. These results indicate that bacterial communities of eggshells and body parts of female hoopoes are at least partially conditioned by the symbiotic community in the uropygial gland. We discuss the importance of these results for understanding this host–microbial mutualism functioning and evolution.     

Sources of variation in uropygial gland size in European birds

Defence mechanisms against parasites and pathogens are some of the most elaborate biological systems in animals. The oily secretion of the avian uropygial gland has been suggested to serve as a chemical defence against feather and eggshell bacteria. Yet, the traits associated with uropygial gland oil production are not well understood. We conducted a phylogenetic analysis comprising 132 European bird species aiming to test: (1) whether life‐history and ecological traits drive gland size evolution by potentially promoting microbial infestation and (2) how these traits affects change in the gland size throughout the annual cycle. We show that the size of the uropygial gland is dynamic (i.e. increasing from the nonbreeding to the breeding season, independent of sex). Furthermore, we found that the year‐round size of the gland was similar between sexes and was correlated with different ecological and life‐history traits promoting microbial infection throughout the annual cycle. During the breeding season, the total eggshell surface area in a clutch correlated significantly and positively with the gland size, suggesting the importance of oil in protecting eggs from microbes. Social species exhibited a larger gland size increase during the breeding season compared to nonsocials; a change that was also predicted by the total eggshell surface area. Aquatic, riparian and non‐migratory species had larger glands than terrestrials and migrants, respectively. The findings of the present study suggest that aquatic environments may promote the production of gland oil, through either the need of waterproofing the plumage and/or defending it against the intensified feather degradation in these moist conditions. Finally, we found a negative effect of the incubation period on uropygial gland size, which may suggest an energetic constraint imposed by other development‐connected costly activities. Our results show that the role of the uropygial gland dynamically varies during the annual cycle, potentially in response to seasonal variation in parasitic infection risk. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 543–563.     

Feather mites and birds: an interaction mediated by uropygial gland size?

Feather mites (Arachnida: Acari: Astigmata) feed mainly on secretions of the uropygial gland of birds. Here, we use analyses corrected for phylogeny and body size to show that there is a positive correlation between the size of this gland and mite abundance in passerine birds at an interspecific level during the breeding season, suggesting that the gland mediates interactions between mites and birds. As predicted on the basis of hypothesized waterproofing and antibiotic functions of uropygial gland secretions, riparian/marsh bird species had larger glands and higher mite loads than birds living in less mesic terrestrial environments. An unexpected pattern was a steeper relationship between mite load and gland size in migratory birds than in residents. If moderate mite loads are beneficial to a host but high loads detrimental, this could create complex selection regimes in which gland size influences mite load and vice versa. Mites may exert selective pressures on gland size of their hosts that has resulted in smaller glands among migratory bird species, suggesting that smaller glands may have evolved in these birds to attenuate a possible detrimental effect of feather mites when present in large numbers.     

Chemical labels differ between two closely related shearwater taxa

Chemical signals may be the basis of interspecific recognition and speciation in many animals. To test whether a chemical label allowing recognition between closely related species exists in seabirds, we investigated two closely related taxa breeding sympatrically at some localities: Cory's and Scopoli's shearwaters. Procellariiform seabirds are ideal for this study because they have a well‐developed olfactory system and unequalled associated capabilities among birds. We analysed and compared the relative volatile compounds composition of the uropygial gland secretions of Cory's and Scopoli's shearwaters. As the volatile components from uropygial secretions might also provide some critical eco‐chemical information about population origin and sex, we also examined variations in the volatile compounds between populations and sexes in Cory's shearwater. The chemical data were obtained using gas chromatography–mass spectrometry techniques looking for the presence of these three particular labels: species, population and gender. We found diagnostic differences in uropygial secretions between the two species of shearwaters and smaller but significant variation between populations of Cory's shearwater in the Atlantic. No significant differences were observed between males and females. Individuals might thus use the chemical variation between species to recognize and mate with conspecifics, especially at localities where both species breed sympatrically. Geographical variation in chemical composition of uropygial secretions suggests that selective forces might vary according to locality, and might represent a key in the species recognition. Further behavioural bioassays are needed to determine whether or not these species labels are signals allowing reproductive isolation between these two taxa. Finally, one of the aims of our study was to test easier methods than freezing for storing uropygial gland secretions in the field. We describe here a new possibility for the storage of uropygial secretion samples at ambient temperature in the field, providing an alternative, simple protocol for the sampling of avian chemosignals.