Experimental old nest material predicts hoopoe Upupa epops eggshell and uropygial gland microbiota

Abstract

Nest re‐use in birds has the potential cost of infection by parasites and pathogens but may also be a source of beneficial symbiotic bacteria transmitted horizontally. Eurasian hoopoes Upupa epops host antibiotic‐producing bacteria in their uropygial gland but only while breeding, which suggests that the nest‐hole may be a source of those symbionts. Interestingly, hoopoes do not build nests, thus might prefer for reproduction nest holes with soft materials from previous reproductions. Here, we tested experimentally this preference by installing in the field new nest boxes that were left empty or filled with either sawdust or a mixture of sawdust and hoopoe's nest material from the previous year. We explored the experimental effect on the composition of the uropygial secretion bacterial community, on eggshell bacterial loads, and on several proxies of reproductive success. Hoopoes bred significantly more often in nest boxes with nest material than in empty ones, but the type of nest material did not affect nest box occupancy. Eggs in nest boxes with old‐soft material harbored higher bacterial density on their shells, and the microbiota of the uropygial secretion of nestlings and females in these nest boxes differed from those in nest boxes without old‐soft material. Moreover, although the experiment did not affect breeding success or related proxies, several operational taxonomic units from female uropygial secretions were positively associated with hatching success. This is the first experimental evidence showing that re‐used nest material affects the bacterial community of the uropygial secretions of hoopoe females. This suggests that the nest material can be a source of strains for their incorporation to both the uropygial gland and eggshell communities, highlighting a possible advantage of nest re‐use previously unconsidered.

Autoclaving Nest-Material Remains Influences the Probability of Ectoparasitism of Nestling Hoopoes (Upupa epops)

“…However, although bacterial density in nest-material of nest-boxes under the control treatment tended to be higher than that of nest-boxes under the experimental treatment, the differences only approached statistical significance. It is worth to mention here that using a similar experimental approach, Díaz-Lora and coauthors [ 27 ] found that bacterial loads on hoopoe eggshells in nest-boxes with nest bacterial remains mixed with sawdust was significantly higher than that of eggshells in nest-boxes with only sawdust. Thus, it is possible that the expected experimental effect on nest bacterial density was more easily detected at the egg stage.…”

“…Our experiment might have affected the bacterial community of the uropygial gland and hence the amount and diversity of volatiles in the nest-box and surroundings. However, previously published experimental evidence strongly suggests that the presence of nest-material remains from previous breeding seasons influences the bacterial community of the uropygial secretion of females [ 27 ]. Therefore, given the strong association between the bacterial community and the volatile profile of uropygial secretions [ 26 ], it is likely that the detected effect on the intensity of ectoparasitism was mediated by changes produced in the bacterial community of the uropygial gland.…”

“…We do not have a plausible explanation for this result. We only may speculate with the possibility that C. hemapterus take their cue from volatiles of particular bacterial strains that hoopoe females acquire when breeding in nests-boxes with material remains from previous reproductions [ 27 ]. This is a possibility to be explored in future works.…”

“…The dimensions of nest-boxes are 35 × 18 × 21 cm (internal height × width × depth), 24 cm (bottom-to-hole height), and 5.5 cm (entrance diameter). Information about the study area is further described elsewhere [ 27 , 37 ].…”

“…Preen glands of breeding females and nestlings host mutualistic bacteria that produce antibiotic substances [ 22 , 23 , 24 , 25 , 26 ] and a variety of malodorous volatiles [ 26 ] that some ectoparasites might use to detect active nests. Furthermore, it has been experimentally demonstrated that nest-material remains from previous hoopoe reproductive events affect the microbial community of the uropygial secretion of adults and nestlings [ 27 ]. Thus, a link between nest bacterial communities and volatiles from symbiotic bacteria likely exists in this species.…”