COMPARATIVE STUDY OF UROPYGIAL GLAND TUFT’S FEATHER MORPHOLOGY AMONGST PARROT SPECIES.
Rob Marshall, B.V.Sc., M.A.C.V.Sc (Avian health)
Tailai O’Brien, B.Business, Cert IV Workplace Trainer, Cert III Captive Animals
Carlingford Animal Hospital, Sydney, Australia
There are no studies documenting the type of tuft’s feathers found on the uropygial gland of parrots. The purpose of our study was to identify the type, colour and dimensions of tuft’s feathers in a variety of parrot species. The study used 40 parrot species from various continents, climatic zones, natural habitats, life history and wild diets. They were categorised according to preen gland tuft feather colour into one of four groups: absent, red, melanised and white. The white group was further subdivided. The first subdivision contained species with long tuft’s feathers relative to body size. The second included those species with tuft’s feathers of regular length. Some parrot species with melanised tuft’s feathers had modified down feathers surrounding the preen gland. Others in this group had specialised semiplumes associated with the preen gland. There was no such finding in parrot species with white tuft’s feathers. This pilot study suggests a possible link between the colour and length of preen gland tuft’s feathers and level of feather maintenance contributed by the preen gland in parrots.
Key words: uropygial gland, preen gland oil, tuft’s feathers, feather structure, semiplume, powder down, grooming behaviour, preening, feather destruction behaviour.
Feathers represent the most complex skin (epidermal) structure of vertebrates due to the precise organisation of a network of barbs and barbules which form the vane (pennaceous portion of feather). The barbules, barbs, calamus and rachis are completely keratinized in birds. Theyare created by a particularly resilient beta-pleated-sheet keratin (beta form) rather than the coiled-coil alpha-helix (alpha form) found in mammalian keratins.1 Although found in a large variety of forms, feathers are all composed of this protein beta-keratin and structurally have the same basic parts and branching arrangement.2 The calamus extends into a central rachis. Along each side of the central rachis are barbs that branch into smaller barbules and interlock together via small hooks.2 The diversity in feathers comes from the evolution of small modifications in this basic branching structure to serve different functions. 2 The feathers of parrots are structurally complex and extraordinarily diverse. Their needs for water repellency may influence the spacing and structure of barbs and barbules.3 Thermodynamics may be critical to the development of downy barbs and the subsequent formation of semiplumes and down feathers.3 Aerodynamics probably influence the twisting of barbules producing the velcro effect that holds the wing feathers tightly together during flight.3 Resistance to abrasion by airborne particles is likely to favour large contour feathers and increased strength of flight feathers.3 Melanin deposits in the keratin increases its strength and thickness of the cortex of the ramus of the barb and of the rachis.3 Feathers need to resist abrasion, degradation by bacteria or fungi and consumption by ectoparasites.2 Similarly, exposure to the damaging effects of ultraviolet radiation necessitates a structure that resists UV damage and protects sensitive underlying tissues.2 Feathers need to be flexible so as to move with the limbs, but also be resilient in order to recover their position and shape.2 In addition to functions such as signalling and counter shading for camouflage, feather colour is thought to play a mechanical role.2 Recent evidence suggests some pigments of bird feathers function to preserve plumage integrity by increasing that resistance of feather keratin to bacterial degradation.4 An increase in melanin is associated with a reduction of feather wear due to abrasion.5 White feathers show more breakage than was expected by chance.5 There are noticeable structural differences in the feathers of the many parrot species. For example, the contour feathers over the fore neck and breast of eclectus parrots (Eclectus roratus) are open barbed. In contrast, the same contour feathers of the Pesquet’s parrots (Psittrichas fulgidus) are tightly barbed. Feather structure has evolved in response to habitat, life cycle behaviours, flight requirements, moult patterns and wild diet.3 These relationships suggest the morphology of feathers is the result of a suite of selection pressures.3 In the wild, it seems grooming behaviours are also the result of evolutionary selection pressures.
The feathers of birds require frequent maintenance to keep them functional. These behaviours, particularly bathing and preening, are nearly universal in birds, although their expression and function vary across species.6 Grooming behaviour varies according to the structure of feathers, habitat, natural behaviours and diet amongst other factors.6 For parrots, we describe feather maintenance as four distinct behaviours: bathing, cleaning, preening and grooming. Preening and grooming are behaviours that take place when the feathers are dry.6 Preen gland oil and powder down feathers play major roles in feather maintenance.7 Most parrot families have powder down feathers and functional preen glands. Broadly speaking, those species that produce powder down feathers and have functional preen glands use the self-cleaning aspects of powder down and protective qualities of preen gland oil, particularly its antibacterial, waterproofing and conditioning functions to maintain their feathers in prime condition.
Bathing removes surface dirt from the feathers. Soaking feathers with water during bathing softens inbuilt dirt to reduce cleaning time and lessen feather abrasion by the beak.4 Birds bathe in still water, rain or dust when they have a need to clean their feathers. Dusting may substitute for water bathing in arid areas, for example galahs (Eolophus roseicapillus) take dust bathes when standing water is not readily available.6 When birds bathe with water or saturate themselves in dust they are actively cleaning their plumage.6 Bathing is an innate physical behaviour in birds and most parrots invest significant energy in this activity. The frequency of bathing varies amongst parrot species. For example, Eclectus parrots and many lorikeet species (Loriidae) cared for in captivity pursue bathing opportunities each day whereas Orange-winged Amazon parrots (Amazonia amazonica), which have no functional preen gland were found to bathe every 4 days.
Cleaning takes place when the feathers are still wet following bathing.6 For birds that do not water bathe each day, light cleaning may take place intermittently throughout the day. The beak is used to find and remove dirt from the feathers. Cleaning is aided by bathing and/or the production of powder down. Psittacines take great care when cleaning their feathers. During the daily process, feather barbs are unzipped to remove trapped dirt, and then re-zipped in a meticulous manner. Powder down feathers provides an uninterrupted supply of cleansing powder. The oily powder produced by down feathers attracts and traps dirt and dust within the plumage. Periodically and especially upon waking, parrots like cockatiels (Nymphicus hollandicus) ruffle themselves to clean their plumage of accumulated grime in a shower of visible bloom.
Preening is the act of applying preen gland oil to the feathers. This action is distinct from cleaning and other grooming behaviours. In captivity, preening is most intensive in species that seek daily baths. In other species, preening is an intermittent daily behaviour. Preening feathers with secretions of the uropygial (preen) gland has been found to regulate feather microbial populations and limit feather abrasion and infections.7 Preening protects feather microstructure from external damage and restores feather durability by moisturising the surfaces of feathers with preen gland oil.7 Not all parrots preen. For example, species of Amazona genera do not show preening behaviour because they lack functional preen glands. They rely upon rainwater and powder down to maintain their feathers. Feathers are dry and cleaned before preening takes place. Preening is a methodical behaviour. The bird rubs the beak, face and head over the preen gland tuft in a quick series of forceful repetitive movements to collect the preen oil. During the procedure, they contort themselves in an effort to spread as much oil as possible on their face, beak and over their head. The oil is then smeared over feather surfaces including the remiges and retrices (flight feathers) with equally bizarre twists and turns. The preening process is often interrupted and rarely completed in a single session. Preening will start in the morning and be repeated at intervals during the day until all feathers have been suitably coated.
Grooming is the least active form of feather maintenance. It is an irregular behaviour that includes light cleaning, tidying of feathers and ruffing. Grooming returns misplaced feathers and barbs to their proper position. It represents ongoing feather maintenance and usually takes place after meals but may also take place throughout the day whenever feathers need tidying.
Powder down feathers are modified down feathers present in most parrots to differing degrees.5 These specialised feathers are typically scattered among ordinary down feathers.5 Some species, including Mealy amazon (Amazona farinose) and African grey parrots (Psittacus erithacus) produce copious amounts of powder down.6 The powder down feathers are most developed in white cockatoos, notably sulphur-crested cockatoo (Cacatua galerita galerita), black cockatoos such as yellow -tailed black cockatoo (Calyptorhynchus funereus) and cockatiels (Nymphicus hollandicus). The powder downs of these species are numerous, 2-3mm wide and 4-8mm long rigid sheathed-feathers fixed against the skin in multiple organised tracts (pterylae) over the rump, known as the powder down bed. Desert dwelling princess parrots (Polytelis alexandrae) have 3-4 flexible 2 mm wide and 5-7mm long powder down feathers scattered across each side of the rump. Powder downs grow continuously in healthy birds. They are not moulted.6 They disintegrate from the distal end as they grow shedding a talcum-like white powder.5 They are different from ordinary feathers that are chiefly geared to synthesise structural proteins such as beta keratin.3 Frozen sections show the pulp and epithelia to be rich in neutral lipids.3 It is not yet known if lipids are sequestered within the mature powder or synthesized and secreted by parts of the growing feather.3 Powder downs produce a notable amount of lipoid material during the keratinisation process.3 The conditioning lipid content and self-cleansing function of down powder may complement the feather protection afforded by preen gland oil. In view of the continuous growth, powder downs provide an uninterrupted supply of the lipid-cell complex forming the powder. Some researchers consider powder downs as glandular structures that are everted out rather than having the typical anatomical profile of an invaginated structure as presented by the uropygial gland.7 Eclectus parrots and lorikeets are two of the few parrot species that do not have powder downs. They maintain their feathers by bathing, preening and grooming behaviours.
The preen gland is located dorsally over the caudal vertebrae at the base of the tail.7 It has two storage lobes in parrots with ducts leading from the secretory tissue to a nipple-like papilla. Its sebaceous secretion is expelled under beak or head pressure during the preening process through two orifices at the end of the papilla onto a tuft of circlet feathers (tuft’s feathers).7 The innervation, mode of secretion and expulsion of preen gland oil from the papilla remains poorly understood. The preen gland produces a large amount of volatile and non-volatile compounds in the form of an oleaginous (waxy-oily) material called preen gland oil.7 Notably it specialises in the synthesis of lipids. The waterproofing and conditioning properties of these structurally important lipids are clearly essential for feather durability, as they are involved in maintaining strong feather microstructure and feather suppleness.7 The preen gland also produces volatile chemicals (pheromones) used by birds in social communication and mate selection.7 Preen gland oil contains antimicrobial and antifungal compounds that possibly guard against feather degradation.7 One of the most relevant functions of the preen gland is to maintain feather structure as a means of preserving its waterproofing properties.7 The gland can be difficult to locate in parrots as it is hidden under the skin in a bed of fat beneath the tail contour feathers and in between underdown feathers. The gland is found by lifting the tail contour feathers then looking cranially towards the base of the tail flight feathers where the tuft’s feathers will be seen. White tuft’s feathers are typically more visible than melanised ones. Preen gland tuft’s feathers have been described as specialised miniaturised plumulaceous (down) feathers.7 The calamus of each feather is firmly embedded into the end of the papilla.7 The tuft’s feathers have elongated barbules with multiple nodal prongs along their length.7 This type of feather cannot form vanes. Instead the barbules clump together in an organised fashion to produce a wick-like feather tuft that holds the waxy secretion of the preen gland.7 The nodal prongs increase the oil carrying capacity of the tuft.7 The prongs help to create a fan-like spatial arrangement to each tuft’s feather. This configuration retains capillarate action and provides a large surface area for economic application of preen gland oil.
Materials and methods
We used 40 different parrot species from various continents, climatic zones, natural habitats, life history and wild diets. At least 3 individuals of each species were examined. The tuft’s feathers were examined in situ and after manual extraction. Their colour and length relative to body size were noted. For each species, the feathers were dry mounted on microscope slides for magnifying and microscopic examination. The tuft’s feathers were categorised by these observation into one of four groups: absent, red, melanised and white. The white group was further subdivided. The first subdivision contained species with long tuft’s feathers relative to their body size. The second included those species with tuft’s feathers of regular length.
Preen gland tuft’s feathers were observed in all studied groups except those species belonging to the genus Amazona. All parrot species examined had 9-13 tuft’s feathers observable without magnification. Microscopically, the tuft’s feathers were structurally similar across all studied species. The feathers were classified as semiplumes having elongated nodal barbules with multiple segmented prongs along their length. Four categories of tuft’s feathers were noted: absent, red, melanised and white.
Blue fronted amazon (Amazona aestival), yellow headed amazon (Amazona aestiva aestival) and Cuban amazon (Amazona leucocephala), which are representative of the first group had no tuft’s feathers because they lack a functional preen gland.
Red tuft’s feathers were found in galahs (Eolophus roseicapillus). This was the only parrot species in this study to have red preen gland tufts. A circular arrangement of red semiplumes was observed surrounding the preen gland. The significance of the red tuft’s feather and the specialised semiplumes that surround the preen gland is not yet known. Galahs live across vast dry areas of central Australia. They have a highly developed powder down bed and regularly dust bath in the wild. The red feathering associated with the preen gland of galahs may be related to or determined by the harsh conditions of central Australia.
The third group contained 7 species with melanised tuft’s feathers. The species in this group includes eclectus parrot (Eclectus roratus), red-tailed black cockatoo (Calyptorhynchus magnificus), yellow-tailed black cockatoo (Calyptorhynchus funereus), crimson rosella (Platycercus elegans), superb parrot (Polytelis swainsonii), black-capped lory (Lorius lory)) and nanday conure (Aratinga nenday). Melanin pigmentation strengthens feathers to reduce wear from abrasion.5 Melanised tuft’s feathers suggest these species preen more frequently than those species with white preen gland tufts and are therefore dependent upon preen gland oil for plumage maintenance. This does not necessarily mean that these species are totally reliant upon preen oil for proper feather maintenance. Contained in this group are eclectus parrots that do not produce powder down, and red-tailed and yellow-tailed black cockatoos that have highly developed powder downs concentrated over the rump area. One of the most relevant functions of the uropygial gland is to maintain the feather structure as a means of preserving its waterproofing qualities.8 In this regard, preen oil is crucial to feather maintenance in eclectus parrots. The tropical climate in which eclectus parrots live is hot, humid and interrupted by heavy downpours especially throughout the wet season. This species is known to bath more frequently than other parrots largely due to a need to wash away a wild diet of fruit pulp that sticks to their face and neck feathers. Their feathers are continually exposed to moisture. Powder down is an inappropriate means of feather maintenance in such a wet environment whereas the water-proofing and antimicrobial qualities of preen oil are crucial. The melanistic and voluminous tuft’s feathers and complex array of specialised down feathers that surround the preen gland attest to the importance of preen oil for feather maintenance in eclectus parrots. Crimson rosellas and superb parrots have a similarly sophisticated assemblage of specialised down feathers surrounding their melanised preen gland tuft’s feathers. These temperate parrots also live in a wet environment characterised by heavy seasonal dew fall and freezing temperatures. Red-tailed and yellow-tailed black cockatoos have melanised preen gland tuft’s feathers and specialised powder down beds, which represent the extreme forms of each method of plumage maintenance. These species inhabit a wide area of diverse habitats exposing them to heavy dew fall, rain and freezing temperatures in winter and long periods of dry heat in summer. These alternating climatic opposites may explain a need for two extreme systems of feather maintenance.
Eclectus parrots and crimson rosella have a convoluted array of specialised modified down feathers surrounding and covering the preen gland. Nanday conures have fan-like semiplumes covering the preen gland. These feathers were not present in any of the other species under study. The function of these auxiliary preen gland feathers is not known.
The final group includes 30 species with white tufted preen glands. This group was divided into species with long tuft’s feathers relative to body size and those with regular length tuft’s feathers. Differences in length of tuft’s feathers between aquatic and terrestrial bird species has been attributed to a greater amount of preen gland secretion due to a greater exposure to water.9 We contend that parrot species with long tuft’s feathers are likely to be exposed to moisture in some form.
The following 6 species have long white tuft’s feathers relative to body size: twenty-eight parrot (Barnadius zonarius semitorquatus), green cheeked conure (Pyrrhura molinae), red-rumped parrot (Psephotus haematonotus), hooded parrot (Psephotus chrysopterygius dissimilis), green cheeked conure (Pyrrhura molinae) and budgerigar (Melopsittacus undulates). Notably the Australian species in this subdivision are all grass parrots that forage on the ground in habitats with heavy seasonal dewfall. Long tuft’s feathers may suggest these species gain benefits from the waterproofing qualities of preen oil. The plumage of these grassland species is frequently exposed to moisture whilst foraging amongst wet grass during times of seasonal dewfall. Wet plumage hinders flight and exposes small birds to predation.10 Long tuft’s feathers provide these birds with the potential to increase the water repellent qualities of their feathers when seasonally required. The white tuft’s feathers of red-rump parrots, which weigh 60-65gm were the longest relative to body size of any bird within this final study group. The tuft’s feathers of the 30-40 gm wild budgerigar are also long relative to its body size. Budgerigars inhabit vast arid areas of central Australia. In common with all desert and semi-desert regions temperatures show a high diurnal range. Marked changes in humidity may occur during all months of the year across these areas. During the day, humidity is low, but at night the temperature may fall to the dew point and the air becomes saturated with water vapour. Dew condenses on leaves of grasses and trees. The plumage becomes wet when budgerigars forage because of dewfall on these plants. The increased holding capacity of the long tuft’s feathers of budgerigar may fulfil additional functions beyond waterproofing. The uropygial gland appears to have several non-mutually exclusive functions in birds.8 A growing body of work shows the important implications of volatile compounds in preen oil with regard to social communication in birds.8 Moreover, preen oil clearly alters plumage colouration.8 Budgerigars are opportunistic breeders that respond to rain. Rain is scarce and an unpredictable event across central Australia. Following significant rainfall, budgerigars respond with a prenuptial head moult. Preening behaviour may increase during this short moult period as a means to enhance plumage brightness especially regarding ornamental traits. Structural colours such as violet would benefit most from preen oil. The violet cheek patches of budgerigars are thought to be involved in mate selection as they signal some aspect of male quality. The long tuft’s feathers of budgerigars may be involved in enhancing sexually selected traits as well as providing waterproofing function.
The white tuft’s feathers of the following 23 species are categorised to be of regular length: Australian king parrot (Alisterus scapularis), red-winged parrot (Aprosmictus erythropterus erythropterus), blue and gold macaw (Ara arauna), scarlet macaw (Ara macao), jandaya conure (Aratinga jandaya), peach-faced lovebird (Agapornis roseicollis), Gang-gang cockatoo (Callocephalon fimbriatum), sulphur-crested cockatoo (Cacatua galerita galerita), Major Mitchell cockatoo (Cacatua leadbeateri), little corella (Cacatua sanguinea), long-billed corella (Cacatua tenuirostris), Hahn or northern red-shouldered macaw (Diopsittaca noblis), Pacific parrotlet (Forpus coelestis), musk lorikeet (Glossopsitta concinna), quaker or monk parrot (Myiopsitta monachus), cockatiel (Nymphicus hollandicus), black-headed caique (Pionites melanocephala), princess parrot (Polytelis alexandrae), blue bonnet (Psethotus haematogaster), rose-ringed parakeet (Psiittacula krameri), alexandrine parakeet (Psiittacula eupatria), african grey (Psittacus erithacus), green cheeked conure (Pyrrhura molinae) and rainbow lory (Trichoglossus haematodus) are included in this group. A possible explanation for the regular length tuft’s feathers of these species is that preen oil plays a lesser auxilary role to powder down for feather maintenance.
In conclusion, this parrot study suggests a possible link between the colour and length of preen gland tuft’s feathers and level of feather maintenance contributed by the preen gland.
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