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Preening as a Vehicle for Key Bacteria in Hoopoes

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Abstract

Oily secretions produced in the uropygial gland of incubating female hoopoes contain antimicrobial-producing bacteria that prevent feathers from degradation and eggs from pathogenic infection. Using the beak, females collect the uropygial gland secretion and smear it directly on the eggshells and brood patch. Thus, some bacterial strains detected in the secretion should also be present on the eggshell, beak, and brood patch. To characterize these bacterial communities, we used Automatic Ribosomal Intergenic Spacer Analysis (ARISA), which distinguishes between taxonomically different bacterial strains (i.e. different operational taxonomic units [OTUs]) by the size of the sequence amplified. We identified a total of 146 different OTUs with sizes between 139 and 999 bp. Of these OTUs, 124 were detected in the uropygial oil, 106 on the beak surface, 97 on the brood patch, and 98 on the eggshell. The highest richness of OTUs appeared in the uropygial oil samples. Moreover, the detection of some OTUs on the beak, brood patch, and eggshells of particular nests depended on these OTUs being present in the uropygial oil of the female. These results agree with the hypothesis that symbiotic bacteria are transmitted from the uropygial gland to beak, brood patch, and eggshell surfaces, opening the possibility that the bacterial community of the secretion plays a central role in determining the communities of special hoopoe eggshell structures (i.e., crypts) that, soon after hatching, are filled with uropygial oil, thereby protecting embryos from pathogens.

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Acknowledgments

We thank Estefanía López Hernández and Olga Corona Forero for the help in laboratory work and Ana Belén García, Jonathan Romero Masegosa, Manuel Soto Cárdenas, Magdalena Ruiz-Rodríguez, and Jorge Doña Reguera for the help in caring of captive hoopoes. Laura Arco, Emilio Pagani, Juan Manuel Peralta-Sánchez, and Tomás Perez Contreras helped with the field work. The manuscript benefits from comments on a previous version by Juan Manuel Peralta-Sánchez and Magdalena Ruiz-Rodríguez. Support by funding was provided by Spanish Ministerio de Economía y Competitividad, European funds (FEDER) (CGL2013-48193-C3-1-P, CGL2013-48193-C3-3-P) and Junta de Andalucía (P09-RNM-4557). AM-G had a predoctoral grant from the Junta de Andalucía (P09-RNM-4557).

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Authors and Affiliations

  1. Estación Experimental de Zonas Áridas (CSIC), E-04120, Almería, Spain

    Ángela Martínez-García & Juan J. Soler

  2. Departamento de Microbiología, Universidad de Granada, E-18071, Granada, Spain

    Sonia M. Rodríguez-Ruano, Manuel Martínez-Bueno & Antonio Manuel Martín-Platero

  3. C/Badolatosa 50, 41560, Estepa, Sevilla, Spain

    Natalia Juárez-García

  4. Departamento de Zoología, Universidad de Granada, E-18071, Granada, Spain

    Manuel Martín-Vivaldi

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  1. Ángela Martínez-García
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Correspondence to Ángela Martínez-García.

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Appendix 1

Relationships of OTU co-occurrence between pairs of sampled sites (UO vs. B, B vs. BP, BP vs. E, B vs. E, UO vs. E, UO vs. BP) within females, being UO (uropygial oil), B (beak), BP (brood patch) and E (eggshells). The p-values obtained by means of Log-linear analyses were corrected for multiple tests by using FDR methodology. Three of 27 frequent OTUs (139 bp, 171 bp, 219 bp) were specific of uropygial oil (UO) and were not used for this analysis. N represents the number of females in which each OTU was detected in the two sampled sites compared (DOCX 38 kb)

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Martínez-García, Á., Soler, J.J., Rodríguez-Ruano, S.M. et al. Preening as a Vehicle for Key Bacteria in Hoopoes. Microb Ecol 70, 1024–1033 (2015). https://doi.org/10.1007/s00248-015-0636-1

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