Seasonal, sexual and developmental differences in hoopoe Upupa epops preen gland morphology and secretions: evidence for a role of bacteria

Abstract

The uropygial glands of birds serve multiple functions, and there is great interspecific variability in the composition and properties of their secretions. A special case is the secretion in the hoopoes Upupa epops, and green woodhoopoes Phoeniculus purpureus, which, contrary to the commonly white and odourless secretions, are dark with pungent odour. Recently, bacteria have been isolated from glands of both woodhoopoes and hoopoes and here we test the hypothesis that bacteria are responsible of some of the special properties of glands and secretions of this group of birds. We explore natural seasonal changes and intersexual differences in the properties of hoopoe glands and secretions, check the natural occurrence of bacteria within secretions, and analyse the effect of experimental injection of antibiotics on uropygial gland properties. Male glands underwent no seasonal changes, and their secretions were invariably white and odourless, very similar to female glands outside the breeding season. However, in comparison to the uropygial gland of non-breeding females, those of incubating females showed a marked increase in size and volume of secretion produced, which became dark and pungent. All these parameters increased until the hatching date and returned to values similar to those in the prelaying phase towards the end of the nestling period. Nestling glands produced secretions similar to those of females in colour and odour. Gland size of both females and nestlings predicted the amount of secretion produced. Microscopic techniques confirmed the presence of bacteria at high density and in active division in all dark secretions examined. The antibiotic treatment significantly reduced the load of enterococci in nestling glands, did not affect size of glands, but diminished the volume of secretion, which was lighter in colour than that of control nestlings. In nesting females, the experimental injection of antibiotic affected some measurements of gland size and secretion colour. Because the experiment did not affect general health estimates (immunocompetence, body condition or growing) of nestlings, our results suggest that some of the special properties of hoopoe glands are mediated by the presence of symbiotic bacteria.

Environmental Factors Shape the Community of Symbionts in the Hoopoe Uropygial Gland More than Genetic Factors

“…In a natural scenario (nestlings growing in their original nests), nestlings could acquire bacteria from the genetic mother through nest contamination by strains from the adult female (56). Actually, some of the breeding behavior of adult female hoopoes such as egg besmearing with UGS (14,33) or touching offspring with the bill impregnated with secretion may increase the probability of vertical transmission. Such behavior should result in enterococcal symbionts from their gland being abundant in the nest environment, thus easily reaching the developing UG of hatchlings.…”

“…UGS was extracted by inserting the tip of a micropipette (Finpipette; 1 to 10 l) directly through the UG external opening and pipetting several times until the papilla in which the secretion is stored was emptied (33). To reduce the probability of contamination, we wore new latex gloves for each extraction.…”

“…Symbiotic bacteria are present in the dark secretions of the UG (referred to here as the UGS) of hoopoes, which are produced by incubating/brooding adult females and nestlings, but have not been found in the white secretions produced by males and nonbreeding adult females (14,33). Bacterial symbionts are likely responsible for particularities such as brown color, malodor, and antimicrobial properties (14,33,34). The UG microbial community in adult females could be fixed during their lives, or, alternatively, new symbionts could colonize their UG, which would result in the presence of different microbial communities in the course of successive breeding seasons.…”

Context-dependent symbioses and their potential roles in wildlife diseases

“…In European hoopoes (Upupa epops) and green woodhoopoes (Phoeniculus purpureus), females exude dark, pungent secretions from their uropygial gland, but only during the short period when they are incubating eggs [29]. These secretions contain antibiotics that inhibit bacterial pathogens.…”

“…The antibiotics are produced by mutualist Enterococcus bacteria that occur in the secretions [30,31]. Eggs and/or nestlings are presumably protected from infection by these secretions [29,32]. It is not known how the birds regulate the change in secretion type, but non-nesting females and all males produce clear or white secretions, without bacteria, and inactive against pathogens [29].…”