Uropygial Gland Research Articles

Bacteria from the Amycolatopsis genus associated with a toxic bird secrete protective secondary metabolites

Uropygial gland secretions of birds consist of host and bacteria derived compounds and play a major sanitary and feather-protective role. Here we report on our microbiome studies of the New Guinean toxic bird Pachycephala schlegelii and the isolation of a member of the Amycolatopsis genus from the uropygial gland secretions. Bioactivity studies in combination with co-cultures, MALDI imaging and HR-MS/MS-based network analyses unveil the basis of its activity against keratinolytic bacteria and fungal skin pathogens. We trace the protective antimicrobial activity of Amycolatopsis sp. PS_44_ISF1 to the production of rifamycin congeners, ciromicin A and of two yet unreported compound families. We perform NMR and HR-MS/MS studies to determine the relative structures of six members belonging to a yet unreported lipopeptide family of pachycephalamides and of one representative of the demiguisins, a new hexapeptide family. We then use a combination of phylogenomic, transcriptomic and knock-out studies to identify the underlying biosynthetic gene clusters responsible for the production of pachycephalamides and demiguisins. Our metabolomics data allow us to map molecular ion features of the identified metabolites in extracts of P. schlegelii feathers, verifying their presence in the ecological setting where they exert their presumed active role for hosts. Our study shows that members of the Actinomycetota may play a role in avian feather protection.

Microbial DNA extraction method for avian feces and preen oil from diverse species.

As DNA sequencing technology continues to rapidly improve, studies investigating the microbial communities of host organisms (i.e., microbiota) are becoming not only more popular but also more financially accessible. Across many taxa, microbiomes can have important impacts on organismal health and fitness. To evaluate the microbial community composition of a particular microbiome, microbial DNA must be successfully extracted. Fecal samples are often easy to collect and are a good source of gut microbial DNA. Additionally, interest in the avian preen gland microbiome is rapidly growing, due to the importance of preen oil for many aspects of avian life. Microbial DNA extractions from avian fecal and preen oil samples present multiple challenges, however. Here, we describe a modified PrepMan Ultra Sample Preparation Reagent microbial DNA extraction method that is less expensive than other commonly used methodologies and is highly effective for both fecal and preen oil samples collected from a broad range of avian species. We expect our method will facilitate microbial DNA extractions from multiple avian microbiome reservoirs, which have previously proved difficult and expensive. Our method therefore increases the feasibility of future studies of avian host microbiomes.

Social environment influences microbiota and potentially pathogenic bacterial communities on the skin of developing birds

BackgroundAnimal bacterial symbionts are established early in life, either through vertical transmission and/or by horizontal transmission from both the physical and the social environment, such as direct contact with con- or heterospecifics. The social environment particularly can influence the acquisition of both mutualistic and pathogenic bacteria, with consequences for the stability of symbiotic communities. However, segregating the effects of the shared physical environment from those of the social interactions is challenging, limiting our current knowledge on the role of the social environment in structuring bacterial communities in wild animals. Here, we take advantage of the avian brood-parasite system of Eurasian magpies (Pica pica) and great spotted cuckoos (Clamator glandarius) to explore how the interspecific social environment (magpie nestlings developing with or without heterospecifics) affects bacterial communities on uropygial gland skin.ResultsWe demonstrated interspecific differences in bacterial community compositions in members of the two species when growing up in monospecific nests. However, the bacterial community of magpies in heterospecific nests was richer, more diverse, and more similar to their cuckoo nest-mates than when growing up in monospecific nests. These patterns were alike for the subset of microbes that could be considered core, but when looking at the subset of potentially pathogenic bacterial genera, cuckoo presence reduced the relative abundance of potentially pathogenic bacterial genera on magpies.ConclusionsOur findings highlight the role of social interactions in shaping the assembly of the avian skin bacterial communities during the nestling period, as exemplified in a brood parasite—host system.

What do we really know about the water repellency of feathers?

Feathers are complex integument structures that provide birds with many functions. They are vital to a bird's survival, fundamental to their visual displays, and responsible for the evolutionary radiation of the avian class. Feathers provide a protective barrier for the body; their water repellency is a key feature. Despite hundreds of years of ornithological research, the available literature on how feathers repel water is both limited and puzzling. Most hypotheses from the early 1900s suggested uropygial gland oil provided feathers with a hydrophobic coating. Subsequent studies showed that the feather's hierarchical structure creates a porous substrate that readily repels water with or without oil. Numerous studies and methods have been published attempting to explain, quantify, and compare the water repellency of feathers. Many overlook the role of barbules and the effect of their variation, which both likely play a crucial part in water repellency. The goal of this paper is to synthesize this research to better understand what has been done, what makes sense, and more importantly, what is missing. Previous reviews on this subject are mostly over 30 years old and did not use modern methods for systematic review. Here, we performed a systematic review to capture all relevant published papers on feather water repellency. We emphasize the crucial role of barbules in feather water repellency and why their morphological variation should not be ignored. We answer the question, what do we really know about the water repellency of feathers?

Morphometric, macroscopic and microscopic investigation of glandulae uropygiale in turkeys (Meleagris gallopavo).

This study was carried out to investigate the macroanatomical, morphometric, histological, and electron microscopic characteristics of the uropygial gland in adult male and female turkeys (Meleagris gallapovo).

The Impact of Avian Haemosporidian Infection on Feather Quality and Feather Growth Rate of Migratory Passerines.

Bird feathers have several functions, including flight, insulation, communication, and camouflage. Since feathers degrade over time, birds need to moult regularly to maintain these functions. However, environmental factors like food scarcity, stress, and parasite infections can affect feather quality and moult speed. This study examined the impact of avian haemosporidian infection and uropygial gland volume, as well as feather quality and feather growth rate in two migratory hirundine species captured in southwestern Spain-the house martin (Delichon urbicum) and sand martin (Riparia riparia). Our findings showed that the prevalence of infection varied among species, with house martins having the highest rates, possibly due to their larger colony size. Moreover, haemosporidian infection had a different impact on each species; infected house martins exhibited lower feather quality than healthy individuals, although this outcome was not observed in sand martins. Furthermore, no effect of infection on feather growth rate was observed in both hirundinids. Additionally, feather growth rate only correlated positively with feather quality in house martins. Finally, no link was observed between uropygial gland volume and feather quality or feather growth rate in any of the species in this study. These findings highlight the effect of haemosporidian infections on the plumage of migratory birds, marking, for the first time, how avian haemosporidian infection is shown to adversely impact feather quality. Even so, further research is needed to explore these relationships more deeply.

Exploring avian exposure to parent polycyclic aromatic hydrocarbons (PAHs): Using the common eider Somateria mollissima in a global context

Compared to other organic contaminants, birds are rarely studied for their exposure to polycyclic aromatic hydrocarbons (PAHs), mainly due to their effective metabolization of parent PAHs. However, as some studies suggest, exposure to PAHs may result in adverse health effects including decreased survival, especially following oil spills. In the present study, we analyzed samples from a sea duck, the common eider Somateria mollissima including feathers, preen oil, blood, liver and bile, to evaluate whether non- lethally collected samples could be reliably used for avian biomonitoring strategies. Phenanthrene was the only individual PAH detected across sample types, with the highest concentration found in preen gland and the lowest in blood. Significant differences in concentrations were observed between bile vs preen gland and liver vs preen gland, while for most compounds neither blood nor feathers showed detectable levels of parent PAHs. Therefore, the utility of those sample types for PAH exposure assessment may be limited and should be interpreted with caution, moreover as several physiological factors may affect them. Additionally, we also provide a comparison with the available literature to review current avian PAH exposure assessment and outline future research focused needs.

Exploring the morphology of the glandula uropygialis in Denizli rooster: 3 tesla MRI and histological investigation

The aim of this study was to examine the preen gland (uropygial gland) of Denizli rooster, an endemic species for Turkey, both macroscopic and by magnetic resonance imaging and to present its histological formation. Five adult male subjects were used for this study. Although some of the findings of the preen gland in Denizli rooster were quite similar to the previous studies on the various avian species, widely branching secondary sinuses of the both two lobes of the gland were formed different from those. It was observed that the sinuses of these two lobes were connected to each other by forming passageway at the isthmus region of the gland. MR images showed bright white hyper-echoic features due to high fat secretion of the preen gland. Therefore, it was determined that the preen gland could be easily isolated from the surrounding tissues. It was also observed in the MR images that the gland in the Denizli cock has a pair of symmetrical bilateral lobes and is located on both sides. This connection gave rise to thought that the problems occurred by the blockage of the one of the primary canals can be solved by the compensation of another canal connected through this passageway. Thus, the secretion of the gland could be maintained properly.

No sex difference in preen oil chemical composition during incubation in Kentish plovers.

Preen oil, the secretion from the uropygial gland of birds, may have a specific function in incubation. Consistent with this, during incubation, the chemical composition of preen oil is more likely to differ between sexes in species where only one sex incubates than in species where both sexes incubate. In this study, we tested the generality of this apparent difference, by investigating sex differences in the preen oil composition of a shorebird species, the Kentish plover (Anarhynchus, formerly Charadrius, alexandrinus). As both sexes incubate in this species, we predicted the absence of sex differences in preen oil composition during incubation. In the field, we sampled preen oil from nine females and 11 males during incubation, which we analysed with gas chromatography-mass spectrometry (GC-MS). Consistent with predictions, we found no sex difference in preen oil composition, neither in beta diversity (Bray-Curtis dissimilarities) nor in alpha diversity (Shannon index and number of substances). Based on these results, we cannot conclude whether preen oil has a function during incubation in Kentish plovers. Still, we discuss hypothetical roles, such as olfactory crypsis, protection against ectoparasites or olfactory intraspecific communication, which remain to be tested.

Uropygial gland size increases isometrically with body size in 35 North American bird species

Abstract The uropygial gland and the oils it produces have been shown to serve important functions in many bird species including plumage maintenance and chemical communication. Previous species comparisons of uropygial gland size have only been conducted in South American and European birds and have found little to no phylogenetic signal. Here, we document uropygial gland measurements of 34 different passerines, 1 hybrid chickadee population, and 1 Piciformes in eastern Pennsylvania, most of which are reported for the first time. Uropygial gland size is positively related to overall body size, controlling for phylogenetic relatedness. We show a significant phylogenetic signal of relative uropygial gland size and many of the species with the largest gland sizes belong to the Paridae. Overall, females show a nonsignificant but slight trend of larger relative uropygial gland sizes than males. This effect is stronger in some species than others and can also be seasonally dependent. We found no effect of relative total eggshell surface area or nest location on relative uropygial gland size. Together our results provide the first documentation of uropygial gland sizes in many of these North American species and provide interesting insight into factors influencing relative gland size including sex, season, and species.

Macroscopic and microscopic characteristics of uropygial gland of budgerigars (Melopsittacus undulatus)

Objective: This study was carried out to investigate the anatomical, morphometric, topographic, and histological features of the uropygial gland in adult male and female budgerigars (Melopsittacus undulatus).
 Material-Method: For this study, the glandula uropygialis of fourteen adult budgerigars (7 male, 7 female) were used in the study. This glandular structure located between the caudal vertebrae and pygostyle was removed by careful dissection. Morphological and histological characteristics of the dissected glandula uropygialis were determined. In addition, morphometric measurements and index calculations were performed. Tissue samples taken to determine the histological structure of the gland were stained with Hematoxylin & Eosin (H&E), Masson Trichrome's and Periodic Acid Schiff-Alcian Blue.
 Result: In the study, it was determined that the gland structure was heart shaped and consisted of two lobes, a papilla and a draining duct system. Uropygial gland weight was determined as 1.57±0.96 g in male birds and 1.52±0.09 g in female birds. As a result of the statistical evaluation, there were significant differences between the sexes in the parameters of lobe width (P

Individual and environmental factors influencing preen gland's morphology and physiology in the barn owl Tyto alba

Avian preen gland helps birds cope with their environment, although its overall functioning remains unclear. We shed light on the complexity of the preen gland's functioning by studying how multiple factors associate with gland morphology (size and shape) and physiology (wax secreted) in barn owls Tyto alba. Individual factors (sex, breeding stage, body condition) were more important predictors of preen gland than environmental factors (temperature, humidity, brood size). Sex, depending on breeding stage in adults, influenced preen gland traits, pointing to the preen gland's regulation by sex hormones and a greater pressure on females to protect their eggs, offspring and themselves throughout reproduction. Adults and fledglings in better condition had larger glands, pointing to the existence of physiological costs. Temperature and humidity, in interaction with plumage coloration, also influenced but to a lesser extent preen gland traits, suggesting that melanin pigmentation and preen gland act as superseding mechanisms when protecting plumage against microorganisms. Finally, fledglings living in larger broods had larger glands, suggesting a role for the social environment in preen gland's functioning. Overall, our study supports the idea that preen gland functions in diverse biological contexts within the same species and is thus subject to multiple selective pressures.

Melanin-based plumage coloration and melanin content in organs in the barn owl

Although the evolutionary ecology of melanin pigments and melanin-based coloration has been studied in great details, particularly in birds, little is known about the function of melanin stored inside the body. In the barn owl Tyto alba, in which individuals vary in the degree of reddish pheomelanin-based coloration and in the size of black eumelanic feather spots, we measured the concentration in melanin pigments in seven organs. The eyes had by far the most melanin then the skin, pectoral muscle, heart, liver, trachea, and uropygial gland. The concentration in eumelanin was not necessarily correlated with the concentration in pheomelanin suggesting that their production can be regulated independently from each other. Redder barn owls had more pheomelanin in the skin and uropygial gland than white owls, while owls displaying larger black feather spots had more eumelanin in the skin than small-spotted owls. More data are required to evaluate whether melanin-based traits can evolve as an indirect response to selection exerted on melanin deposition in organs.

Host space, not energy or symbiont size, constrains feather mite abundance across passerine bird species.

Comprehending symbiont abundance among host species is a major ecological endeavour, and the metabolic theory of ecology has been proposed to understand what constrains symbiont populations. We parameterized metabolic theory equations to investigate how bird species' body size and the body size of their feather mites relate to mite abundance according to four potential energy (uropygial gland size) and space constraints (wing area, total length of barbs and number of feather barbs). Predictions were compared with the empirical scaling of feather mite abundance across 106 passerine bird species (26,604 individual birds sampled), using phylogenetic modelling and quantile regression. Feather mite abundance was strongly constrained by host space (number of feather barbs) but not by energy. Moreover, feather mite species' body size was unrelated to the body size of their host species. We discuss the implications of our results for our understanding of the bird-feather mite system and for symbiont abundance in general.

Preening cups increase apparent wet preening behaviors, but have no impact on other behaviors, body condition, growth, or body morphometrics of grow-out Pekin ducks

Preening cups may be a form of open water that would allow ducks to express preening behaviors. We set out to test the hypothesis that preening cups would not have detrimental effects on ducks or their environment. Control pens (N=6, 65 ducks/pen) had nipple lines while experimental pens (N=6, 65 ducks/pen) had the same nipple line plus one preening cup (PC). Body weights of 30 ducks per pen, and body condition scores on 50 ducks per pen were recorded weekly. On d 18 and 43, 5 ducks per pen were euthanized and their spleens, Bursas, liver, and uropygial glands were weighed. Behavior data were collected using scan sampling with video being recorded for 72 continuous hours at 4 different ages: 25 d, 30 d, 36 d, and 40 d. Body morphometrics were analyzed by 2-way ANOVA with repeated measures. Body condition scoring was analyzed by Pearson's chi-square. The GLIMMIX procedure (SAS 9.4) was used for behavioral analyses to examine treatment differences in the proportion of ducks performing dry preening, wet preening, eating, drinking, standing, and laying down. Feather pecking, feather picking, preening conspecifics (also known as allopreening), dunking head, and drinking from preening cup were analyzed using PROC LOGISTIC with the Firth bias correction for quasi-complete separation and odds ratios were calculated. More PC ducks housed with PC performed wet preening compared to control ducks (25 d: F1,26=6.90, P=0.0143; 30, 36, and 40 d; F1,78=24.53, P < 0.0001). Ducks in the PC group were also more likely to lay down compared to controls (25 d: F1,33=4.95, P=0.0330). No differences were observed for any other behavior, body condition score, body weight or morphometrics at any age. Although ducks in the preening cup group showed an increase in wet preening, our data suggest that open water is not necessary to maintain feather condition or uropygial gland size.

The abundance and diversity of antibiotic resistance genes in layer chicken ceca is associated with farm enviroment.

Industrialized layer chicken feedlots harbor complex environmental microbial communities that affect the enrichment and exchange of gut bacteria and antibiotic resistance genes (ARGs). However, the contribution of different environmental sources to the gut ARGs of layer chickens is not clear. Here, layer chicken gut and environmental samples (air, water, feed, cage, feather, maternal hen feces, uropygial glands) were collected during the early 3 month period before the laying of eggs, and the source and characteristics of the gut microorganisms and ARGs were analyzed by performing 16S rRNA and metagenomic sequencing. The results showed that the abundances of Bacteroidetes and Actinobacteria in cecum of layer chickens gradually increased, while that of Proteobacteria decreased with age, and the number and relative abundance of ARGs decreased significantly with age. On day 5, 57% of the layer chicken cecal ARGs were from feather samples, and 30% were from cage samples. Subsequently, the contribution of cage ARGs became progressively more prominent over time. At days 30 and 57, the contribution of cage ARGs to the chick cecal ARGs reached 63.3 and 69.5%, respectively. The bacterial community composition (especially the abundances of Klebsiella pneumoniae and Escherichia coli) was the major factor impacting the ARG profile. K. pneumoniae and E. coli were mainly transmitted from feathers to the layer chicken cecum, and the contribution rates were 32 and 3.4%, respectively. In addition, we observed the transmission of ARG-carrying bacteria (Bacteroides fragilis) from the cage to the gut, with a contribution rate of 11.5%. It is noteworthy that B. fragilis is an opportunistic pathogen that may cause diarrhea in laying hens. These results can provide reference data for the healthy breeding of layer chickens and the prevention and control of ARG pollution.

Preen oil composition of Pied Flycatchers is similar between partners but differs between sexes and breeding stages

Preen oil, the secretion of the uropygial gland, may be an important source of body odour in birds. By characterizing the chemical composition of preen oil, we can describe the olfactory phenotypes of birds and investigate whether odours could have a function in sexual signalling or other chemical communication. Here we analysed the preen oil of a wild passerine, the European Pied Flycatcher Ficedula hypoleuca, to find out whether it holds socially relevant information. We sampled both the female and male of breeding pairs during nestling rearing to test for sex differences and within‐pair similarity. We additionally sampled the females during incubation to test for changes across breeding stages and for individual repeatability of chemical profiles. Pair mates had similar chemical profiles in comparison with other breeding adults. Furthermore, we found evidence for sex differences and for changes across breeding stages. Notably, the preen oil of females was more diverse and more volatile than that of males, and the preen oil secreted by females during incubation was more volatile than that secreted during nestling rearing. However, we found no evidence for individual repeatability of chemical profiles across breeding stages in females. Our results point towards a function of preen oil in sexual signalling, although other functions should not be excluded. Our study is a first step towards understanding the role of odours in the social life of an important avian model species used in the study of mate choice and sexual selection.

The uropygial gland of the Great Cormorant (Phalacrocorax carbo): II. Biochemical analysis of the uropygial secretion

In contrast to many other water birds, the Great Cormorant, Phalacrocorax carbo (Phalacrocoracidae), shows a typical wing-spreading behavior after diving. This behavior has been linked to the partial wettability of the Cormorant’s feathers based on the unusual structure of the contour feathers. Close to the rachis, these feathers have a closed vane with very densely spaced barbs but have an open vane in more peripheral feather parts. To investigate whether the wettability is connected to the composition of the uropygial gland secretion that is often linked to water repellency of bird feathers, we analyzed the gland secretions of the Great Cormorant and, for comparison, of the Muscovy Duck, Cairina moschata (Anatidae). Using the mass spectrometry techniques, atmospheric solids analysis probe-atmospheric pressure chemical ionization-mass spectrometry (ASAP-APCI-MS) and gas chromatography/mass spectrometry (GC/MS), significant differences in the chemical composition of the secretions were revealed. The Cormorant showed a highly diverse mixture of more than 1000 compounds consisting of methyl-branched aliphatic carboxylic esters with large chain length variability. In contrast, the duck’s secretion is dominated by the two esters octadecyl and eicosyl 2,4,6-trimethyloctanoate. Water contact angle measurements of the secretions showed that the secretion of the Muscovy Duck has higher water repellency than that of the Great Cormorant. Nevertheless, contact angle measurements of feathers before and after removing of feather waxes indicate that these waxes, likely consisting of the uropygial gland secretions, did not influence water repellency of the feathers to a large degree.

Symbiotic microbiota vary with breeding group membership in a highly social joint-nesting bird

Abstract Symbiotic microbes affect the health, fitness, and behavior of their animal hosts, and can even affect the behavior of non-hosts. Living in groups presents numerous benefits and challenges to social animals, including exposure to symbiotic microbes, which can mediate both cooperation and competition. In social mammals, individuals from the same social group tend to share more similar microbes and this social microbiome, the microbial community of all hosts in the same social group, can shape the benefits and costs of group living. In contrast, little is known about the social microbiome of group living birds. We tested the predictions that communally breeding smooth-billed anis (Crotophaga ani) belonging to the same breeding group share more similar microbes and that microbial community composition differs between body regions. To test this, we used 16S rRNA gene sequencing to characterize the preen gland and body feather microbiota of adult birds from 16 breeding groups at a long-term study site in southwestern Puerto Rico. As predicted, individuals from the same breeding group shared more similar microbiota than non-group members and preen gland and body feathers harbored distinct microbial communities. Future research will evaluate whether this social microbiome affects the behavior of group living birds.

Chemical aposematism: the potential for non‐host odours in avian defence

Many birds display plumage coloration and patterns that act as visual aposematic and mimetic signals for predators. Avian aposematism can also be communicated via chemical cues, where so‐called non‐host odours (NHO) emitted from the plumage, the uropygial (preen) gland or other chemical sources denote the status of birds as dangerous or unprofitable hosts for ectoparasitic and haematophagous arthropods. Avian NHO are aposematic signals that in natural concentrations repel nuisance arthropods or inhibit their attraction to hosts, as opposed to being generally unpalatable or toxic to predators. Birds that emit NHO preempt encounters with nuisance arthropods and the pathogens they transmit. Nuisance arthropods that respond to NHO avoid birds that exhibit disabling behavioural, anatomical, physiological and/or chemical defences. As with distinctive plumage patterns that evolved as visual warnings to predators, birds are selected to advertise their non‐host status to nuisance arthropods via distinctive semiochemicals. Short‐chain (C6–C10) aldehydes emitted from the plumage of some birds may act as NHO against a variety of nuisance arthropods. In some birds, the size of the uropygial gland (and presumably its secretory output) is negatively correlated with the degree of ectoparasite infestation or the incidence of malarial infection, thus implicating uropygial secretions in defence against dipteran vectors of haemosporidian pathogens. A field experiment demonstrates that volatiles emanating from the uropygial gland of the Eurasian Hoopoe Upupa epops deter some biting flies. Birds' risky habit of plucking hair from live mammals and incorporating the stolen hair tufts into their nests is hypothesized to serve as a mechanism of appropriating NHO from mammalian skin secretions for nest defence against arthropods. Feathers plucked from heterospecifics and shed snake skins that are incorporated into nests also may emit NHO. Behavioural assays measuring the repellence or attraction‐inhibition of arthropods are needed to elucidate avian NHO. Experimental efforts to elucidate the underlying defences that support avian NHO entail challenges that include the enactment of defences that are variously effective against different arthropods, and the emission of chemical signals that are variously ‘understood’, i.e. avoided, by different arthropods.