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Kiwi) Possess an Uro- Pygial Gland: Anatomy and Pathology

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Kiwi) Possess an Uro- Pygial Gland: Anatomy and Pathology ORIGINAL ARTICLE Eur. J. Anat. 21 (2): 125-139 (2017) Apteryx spp. (Kiwi) possess an uro- pygial gland: Anatomy and pathology Sian M. Reynolds 1,2 , Isabel Castro1, Maurice R. Alley 3, Susan J. Cunning- ham 4 1P.O. Box 11222, Institute of Agriculture and Environment, Massey University, Palmerston North, New Zealand, 2New Zealand Department of Conservation, Haast Awarua Field Centre. P.O. Box 50, Haast 7844, New Zealand, 3P.O. Box 11222, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand, 4Percy FitzPatrick Institute, DST/NRF Centre of Excellence, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa SUMMARY availability of uropygial gland secretion. This was supported by variations in live bird’s gland volume The uropygial gland is a prominent feature of the between two years of sampling. Atrophy of the uro- avian anatomy but there is limited information on pygial gland was seen in two birds in poor condi- its structure and function. The gland is of current tion suggesting that health impacts the functioning interest because it provides a source for volatile of the gland. This finding suggests an adaptive chemicals that can be used by birds in communi- significance for the gland and offers a possible cation. We examined the anatomy of uropygial way for birds to communicate their health status glands in Apteryx for the first time. The gland was through the production or composition of the se- located immediately caudal to the cloaca and sur- cretion. More research is needed to fully under- rounding the coccygeal bone rather than rostral to stand the relationship between the anatomy of the the coccygeal bone and above the posterior free gland in Apteryx and its function, but we propose caudal vertebrae as in other birds. This may ex- that it plays roles in both feather maintenance and plain why it has not been recognised until relatively sociality. recently. Like most uropygial glands Apteryx ’s were bilobar but possessed eight primary sinuses, Key words: Holocrine – Oil gland – Rump gland – each opening through its own orifice in the gland’s Preen gland – Integumentary gland – Apterygidae papilla. Primary ducts were compact and branches of connective tissue extending from the capsule inter- INTRODUCTION nally formed interfollicular septae that were thicker in some areas, grouping follicles into discrete lob- The uropygial gland, also known as the oil gland, ules. Striated muscle was present in the capsule, a rump gland or preen gland (Jacob and Ziswiler, characteristic so far unique to Apteryx that may be 1982; Sadoon, 2011), is one of only three integu- used in controlling the expulsion of secretion. mentary glands found in birds. These skin glands There were significant differences in the architec- are very few when compared to the array of integ- ture of the follicles between species and sexes that umentary glands of reptiles and mammals (Quay, suggest differences in the production, storage and 1972). The evolutionary origins of the uropygial gland are unknown. Homology between the uro- pygial gland and reptilian glands is uncertain (Elder, 1954), although there seem to be phyloge- Corresponding author: Isabel Castro. Institute of Agriculture netic relationships between uropygial gland secre- and Environment, Massey University, P.O. Box 11222, Pal- tions and secretions produced by some reptilian merston North, New Zealand. Phone: +64 6 3569099 ext. 84830; mobile: +64 274491261. E-mail: [email protected] Submitted: 21 September, 2016. Accepted: 11 January, 2017. 125 Apteryx uropygial gland integumentary glands (Quay, 1972). Histologically, secretion contained a chemical which actively at- the avian uropygial gland is most similar to the tracted males during the mating season, and thus mammalian sebaceous gland because of its holo- the composition of the secretion exhibited season- crine structure (Wagner and Brood, 1975; King ality. Likewise Hirao et al. (2009) found that the and McLelland, 1985; Sara et al., 2006). uropygial gland of female chickens ( Gallus gallus Externally, the uropygial gland is visible as an domesticus ) acts as a source of social odour cues. eminence generally located dorsomedially in the The uropygial gland secretion of blue petrels synsachrocaudal area, generally rostral to the py- (Halobaena caerulea ) has an individual signature gostyle and above the posterior free caudal verte- and is used in conspecific recognition (Mardon et brae (Jacob and Ziswiler, 1982). The organ is gen- al., 2011). Starlings ( Sturnus vulgaris ) can identify erally bilobate, with ducts leading from the secreto- the sex of conspecifics by using volatiles in their ry tissue to the papilla and reaching the surface of uropygial gland secretion (Amo et al., 2012). The the body through two or more orifices (Jacob and uropygial gland secretion can be used in cosmetic Ziswiler, 1982). The size, shape, number of circlet colouration ( Phoenicopterus roseus ; Amat et al., feathers, and proportions of the gland cells can 2011) or incorporate toxic, unpalatable, and foul vary greatly (Jacob and Ziswiler, 1982). The pa- smelling chemicals that the bird applies to its plum- renchyma is composed of small follicles with inter- age as a defence mechanism against predators twining ducts leading to primary sinuses. Second- (Martín-Vivaldi et al., 2009; Dumbacher et al., ary sinuses drain secretory product from follicles to 1992; Rajchard, 2010) or microbial parasites primary sinuses for storage (Lucas and Stetten- (Shawkey et al., 2003; Moyer et al., 2003; Chiale heim, 1972). In species in which the gland’s histol- et al., 2014, 2015). ogy has been studied it has four layers of cells To fully understand how the uropygial gland within each follicle (germinative, intermediate, se- works and the possible effect of phylogeny on its cretory and degenerative) (Jacob and Ziswiler, structure and function, it is necessary that we ex- 1982; Chandrasekar et al., 1990; El-Bargeesy et amine the uropygial gland of different bird groups al., 1995; Kale et al., 1999; Sunanda et al., 2001; histologically and through cytochemistry. Recent Sawad, 2006; Onal et al., 2013; Shafiian and Mo- studies for example are analysing information re- bini, 2014; Chiale et al., 2014; Chiale et al., 2016; garding the gland’s structure and chemical produc- Harem et al., 2010; Kozlu, 2011). Many features of tion with the function (Chiale et al., 2014; Chiale et this gland remain a mystery, for example its inner- al., 2015), habitat (Chiale et al., 2016), and phylog- vation, mode of secretion, and the expulsion of the eny of the study birds (Chiale et al., 2014). Of par- secretion from the papilla (Jacob and Ziswiler, ticular interest is the gland of Paleognathous birds 1982). as this group is basal to the entire Aves. Amongst Because of the oily nature of the secretion, wa- the ratites, only adult Apterygidae (five species) terproofing and maintenance of feathers were its and Tinamidae (c. 40 species) are known to have first postulated roles. However, research has uropygial glands (Johnston, 1988; Jacob and shown that the role of the uropygial gland and its Ziswiler, 1982). Interestingly, early authors did not secretion may vary greatly between species. Ex- realize that Apteryx had an uropygial gland until periments by Elder (1954) supported a feather Beddard (1899) examined the gland in three speci- maintenance role (Stettenheim, 2000): removing mens, one of each Apteryx australis , A. haasti and the uropygial gland in ducklings of two species, he A. Mantelli. Beddard (1899) described the gland as showed that the plumage of experimental birds enormous but did not consider it to be bilobar. He deteriorated with age, and survival decreased found that the papilla had two inconspicuous nip- compared to control birds, because the damage to ples and that these had two orifices each. No the plumage exposed them to injury and disease. measurements were taken or other descriptions Salibian and Montalti (2009) did not find any differ- made although the author provides an illustration ence in the size, degree of development of the of a ventral and lateral view of the uropygial gland gland and the bird’s relationship with water, sug- close to the cloaca. In this paper we provide the gesting that it may not have a role in waterproof- first detailed description of the anatomy, morpholo- ing. Giraudeau et al. (2010) experimentally gy, and histology of the uropygial gland of Apteryx , showed that when access to the uropygial gland and provide descriptions of some pathological was prevented for three months in a group of mal- changes that were observed in the uropygial gland lards ( Anas platyrhynchos ), their plumage showed of individuals of three Apteryx species. We discuss lower water-repellence compared to control birds. our findings in terms of the possible function of the Arguably, this may have resulted from deteriora- gland. tion of the plumage with disruption to the micro- structure of the feathers, which is the most com- MATERIALS AND METHODS monly proposed strategy for waterproofing. In some birds the secretion may be involved in External morphometry social cues; Kolattukudy and colleagues in 1987 We measured and photographed twice (in Febru- showed that the female mallard’s uropygial gland ary/March 2008 and March 2009) the uropygial 126 S.M. Reynolds et al. gland of a set of 29 (15 male and 14 female) wild buffered formalin. Each gland was cut in half sagit- brown kiwi ( Apteryx mantelli; all species follow tally between the two papillae (Fig. 1B). One half Burbidge et al. 2002) from Ponui Island, in the was used to produce three pieces: a midline trim- Hauraki Gulf, New Zealand (1770 ha; 36 55’, 175 ming and two lateral trimmings (Fig. 1B) with the 11’E). Nine additional birds (six females and three midline and outermost trimming used for data col- males) were sampled once in 2008. We recorded lection.
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