Microbial Ecology

, Volume 70, Issue 4, pp 1024–1033 | Cite as

Preening as a Vehicle for Key Bacteria in Hoopoes

  • Ángela Martínez-García
  • Juan J. Soler
  • Sonia M. Rodríguez-Ruano
  • Manuel Martínez-Bueno
  • Antonio Manuel Martín-Platero
  • Natalia Juárez-García
  • Manuel Martín-Vivaldi
Host Microbe Interactions
First Online:
Received:
Accepted:

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.

Keywords

Preening Uropygial gland Uropygial oil Hoopoe Symbiotic bacteria ARISA 
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Notes

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).

Supplementary material

248_2015_636_MOESM1_ESM.docx (39 kb)
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)

References

  1. 1.
    Nalepa CA (1994) Nourishment and the origin of termite eusociality. In: Hunt J, Nalepa CA (eds) Nourishment and the evolution of insect societies. Boulder, Colorado, pp 57–104Google Scholar
  2. 2.
    Ley RE, Lozupone CA, Hamady M et al (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788. doi: 10.1038/nrmicro1978 PubMedCentralCrossRefPubMedGoogle Scholar
  3. 3.
    Hill MJ (1997) Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 6:43–45CrossRefGoogle Scholar
  4. 4.
    Macpherson AJ, Harris NL (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4:478–485. doi: 10.1038/nri1373 CrossRefPubMedGoogle Scholar
  5. 5.
    Umesaki Y, Setoyama H, Matsumoto S (1999) Differential roles of segmented filamentous bacteria and clostridia in development of the intestinal immune system. Infect Immun 67:3504PubMedCentralPubMedGoogle Scholar
  6. 6.
    Dillon RJ, Vennard CT, Buckling A, Charnley AK (2005) Diversity of locust gut bacteria protects against pathogen invasion. Ecol Lett 8:1291–1298. doi: 10.1111/j.1461-0248.2005.00828.x CrossRefGoogle Scholar
  7. 7.
    Fons M, Gomez A, Karjalainen T (2000) Mechanisms of colonisation and colonisation resistance of the digestive tract part 2: bacteria/bacteria interactions. Microb Ecol Health Dis 2:240–246. doi: 10.1080/089106000750060495 Google Scholar
  8. 8.
    Barbieri E, Paster BJ, Hughes D et al (2001) Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo pealei (Cephalopoda:Loliginidae). Environ Microbiol 3:151–167CrossRefPubMedGoogle Scholar
  9. 9.
    Currie CR, Poulsen M, Mendenhall J et al (2006) Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311(80):81–83. doi: 10.1126/science.1119744 CrossRefPubMedGoogle Scholar
  10. 10.
    Moran NA (2006) Symbiosis. Curr Biol 16:866–871. doi: 10.1016/j.cub.2006.09.019 CrossRefGoogle Scholar
  11. 11.
    Lindquist N, Barber PH, Weisz JB (2005) Episymbiotic microbes as food and defence for marine isopods: unique symbioses in a hostile environment. Proc R Soc B 272:1209–1216. doi: 10.1098/rspb.2005.3082 PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    Gil-Turnes MS, Hay ME, Fenical W (1989) Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246:116–118. doi: 10.1126/science.2781297 CrossRefPubMedGoogle Scholar
  13. 13.
    Gil-Turnes MS, Fenical W (1992) Embryos of Homarus americanus are protected by epibiotic bacteria. Biol Bull 182:105–108. doi: 10.2307/1542184 CrossRefGoogle Scholar
  14. 14.
    Currie CR, Scott JA, Summerbell RC (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–705CrossRefGoogle Scholar
  15. 15.
    Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A 100:1803–1807. doi: 10.1073/pnas.0335320100 PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    Banning JL, Weddle AL, Wahl GW et al (2008) Antifungal skin bacteria, embryonic survival, and communal nesting in four-toed salamanders, Hemidactylium scutatum. Oecologia 156:423–429. doi: 10.1007/s00442-008-1002-5 CrossRefPubMedGoogle Scholar
  17. 17.
    Martín-Vivaldi M, Soler JJ, Peralta-Sánchez JM et al (2014) Special structures of hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching success. J Anim Ecol 83:1289–1301. doi: 10.1111/1365-2656.12243 CrossRefPubMedGoogle Scholar
  18. 18.
    Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M et al (2008) Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22:864–871. doi: 10.1111/j.1365-2435.2008.01448.x CrossRefGoogle Scholar
  19. 19.
    Martín-Platero AM, Valdivia E, Ruiz-Rodríguez M et al (2006) Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10–3, isolated from the uropygial gland of the hoopoe (Upupa epops). Appl Environ Microbiol 72:4245–4249. doi: 10.1128/AEM.02940-05 PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Law-Brown J, Meyers PR (2003) Enterococcus phoeniculicola sp. nov., a novel member of the enterococci isolated from the uropygial gland of the Red-billed Woodhoopoe, Phoeniculus purpureus. Int J Syst Evol Microbiol 53:683–685. doi: 10.1099/ijs.0.02334-0 CrossRefPubMedGoogle Scholar
  21. 21.
    Mayr G (2007) Avian higher-level phylogeny: well-supported clades and what we can learn from a phylogenetic analysis of 2954 morphological characters. J Zool Syst Evol Res 46:63–72. doi: 10.1111/j.1439-0469.2007.00433.x Google Scholar
  22. 22.
    Martín-Vivaldi M, Ruiz-Rodríguez M, Soler JJ et al (2009) Seasonal, sexual and developmental differences in hoopoe Upupa epops preen gland morphology and secretions: evidence for a role of bacteria. J Avian Biol 40:191–205. doi: 10.1111/j.1600-048X.2009.04393.x CrossRefGoogle Scholar
  23. 23.
    Soler JJ, Martín-Vivaldi M, Peralta-Sánchez JM et al (2014) Hoopoes color their eggs with antimicrobial uropygial secretions. Naturwissenschaften 101:697–705. doi: 10.1007/s00114-014-1201-3 CrossRefPubMedGoogle Scholar
  24. 24.
    Jacob J, Ziswisler V (1982) The uropygial gland. Avian Biol 6:199–314CrossRefGoogle Scholar
  25. 25.
    Reneerkens J, Piersma T, Sinninghe Damsté JS (2002) Sandpipers (Scolopacidae) switch from monoester to diester preen waxes during courtship and incubation, but why? Proc R Soc Lond B 269:2135–2139. doi: 10.1098/rspb.2002.2132 CrossRefGoogle Scholar
  26. 26.
    Delhey K, Peters A, Kempenaers B (2007) Cosmetic coloration in birds: occurrence, function, and evolution. Am Nat 169:145–158. doi: 10.1086/510095 CrossRefGoogle Scholar
  27. 27.
    Delhey K, Peters A, Biedermann PHW, Kempenaers B (2008) Optical properties of the uropygial gland secretion: no evidence for UV cosmetics in birds. Naturwissenschaften 95:939–946. doi: 10.1007/s00114-008-0406-8 CrossRefPubMedGoogle Scholar
  28. 28.
    Lopez-Rull I, Pagan I, Macias Garcia C (2010) Cosmetic enhancement of signal coloration: experimental evidence in the house finch. Behav Ecol 21:781–787. doi: 10.1093/beheco/arq053 CrossRefGoogle Scholar
  29. 29.
    Ruiz-Rodríguez M, Valdivia E, Soler JJ et al (2009) Symbiotic bacteria living in the hoopoe’s uropygial gland prevent feather degradation. J Exp Biol 212:3621–3626. doi: 10.1242/jeb.031336 CrossRefPubMedGoogle Scholar
  30. 30.
    Ruiz-Rodríguez M, Soler JJ, Martín-Vivaldi M et al (2014) Environmental factors shape the community of symbionts in the hoopoe uropygial gland more than genetic factors. Appl Environ Microbiol 80:6714–6723. doi: 10.1128/AEM.02242-14 PubMedCentralCrossRefPubMedGoogle Scholar
  31. 31.
    Sepehri S, Kotlowski R, Bernstein CN, Krause DO (2007) Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease. Inflamm Bowel Dis 13:675–683. doi: 10.1002/ibd.20101 CrossRefPubMedGoogle Scholar
  32. 32.
    Welkie DG, Stevenson DM, Weimer PJ (2010) ARISA analysis of ruminal bacterial community dynamics in lactating dairy cows during the feeding cycle. Anaerobe 16:94–100. doi: 10.1016/j.anaerobe.2009.07.002 CrossRefPubMedGoogle Scholar
  33. 33.
    Porporato EMD, Lo Giudice A, Michaud L et al (2013) Diversity and antibacterial activity of the bacterial communities associated with two Mediterranean sea pens, Pennatula phosphorea and Pteroeides spinosum (Anthozoa: Octocorallia). Microb Ecol 66:701–714. doi: 10.1007/s00248-013-0260-x CrossRefPubMedGoogle Scholar
  34. 34.
    Schöttner S, Hoffmann F, Wild C et al (2009) Inter- and intra-habitat bacterial diversity associated with cold-water corals. ISME J 3:756–759. doi: 10.1038/ismej.2009.15 CrossRefPubMedGoogle Scholar
  35. 35.
    Barbaro L, Couzi L, Bretagnolle V et al (2008) Multi-scale habitat selection and foraging ecology of the eurasian hoopoe (Upupa epops) in pine plantations. Biodivers Conserv 17:1073–1087CrossRefGoogle Scholar
  36. 36.
    Rehsteiner U (1996) Abundance and habitat requirements of the Hoopoe Upupa epops in Extremadura (Spain). Ornithol Beobachter 93:277–287Google Scholar
  37. 37.
    Schaub M, Martinez N, Tagmann-Ioset A et al (2010) Patches of bare ground as a staple commodity for declining ground-foraging insectivorous farmland birds. PLoS One 5, e13115. doi: 10.1371/journal.pone.0013115 PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    Martín-Vivaldi M, Palomino JJ, Soler M, Soler JJ (1999) Determinants of reproductive success in the Hoopoe Upupa epops, a hole-nesting non-passerine bird with asynchronous hatching. Bird Study 46:205–216. doi: 10.1080/00063659909461132 CrossRefGoogle Scholar
  39. 39.
    Bussman J (1950) Zur brutbiologie des wiedehopfes. Ornithol Beobachter 47:141–151Google Scholar
  40. 40.
    Gupta RC, Ahmad I (1993) On the clutch size, egg laying schedule, hatching patterns and stay of nestlings of Indian Hoopoe (Upupa epops). Geobios 20:148–150Google Scholar
  41. 41.
    Cramp S (1998) The complete birds of the Western Palearctic on CD-ROM Software Optimedia. Oxford University Press, OxfordGoogle Scholar
  42. 42.
    Martín-Platero AM, Peralta-Sánchez JM, Soler JJ, Martínez-Bueno M (2010) Chelex-based DNA isolation procedure for the identification of microbial communities of eggshell surfaces. Anal Biochem 397:253–255. doi: 10.1016/j.ab.2009.10.041 CrossRefPubMedGoogle Scholar
  43. 43.
    Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65:4630–4636PubMedCentralPubMedGoogle Scholar
  44. 44.
    Danovaro R, Luna GM, Dell’Anno A, Pietrangeli B (2006) Comparison of two fingerprinting techniques, terminal restriction fragment length polymorphism and automated ribosomal intergenic spacer analysis, for determination of bacterial diversity in aquatic environments. Appl Environ Microbiol 72:5982–5989. doi: 10.1128/AEM.01361-06 PubMedCentralCrossRefPubMedGoogle Scholar
  45. 45.
    Cardinale M, Brusetti L, Quatrini P et al (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70:6147. doi: 10.1128/AEM.70.10.6147 PubMedCentralCrossRefPubMedGoogle Scholar
  46. 46.
    Ramette A (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75:2495–2505. doi: 10.1128/AEM.02409-08 PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Bent SJ, Forney LJ (2008) The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. ISME J 2:689–695. doi: 10.1038/ismej.2008.44 CrossRefPubMedGoogle Scholar
  48. 48.
    Loisel P, Harmand J, Zemb O et al (2006) Denaturing gradient electrophoresis (DGE) and single-strand conformation polymorphism (SSCP) molecular fingerprintings revisited by simulation and used as a tool to measure microbial diversity. Environ Microbiol 8:720–731. doi: 10.1111/j.1462-2920.2005.00950.x CrossRefPubMedGoogle Scholar
  49. 49.
    StatSoft I (2006) STATISTICA (data analysis software system). Version 8. www.statsoft.com
  50. 50.
    Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4 9ppGoogle Scholar
  51. 51.
    Legendre P, Legendre L (1998) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  52. 52.
    Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, URL http://www.R-project.org/
  53. 53.
    Cook MI, Beissinger SR, Toranzos GA, Arendt WJ (2005) Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Lett 8:532–537. doi: 10.1111/j.1461-0248.2005.00748.x CrossRefPubMedGoogle Scholar
  54. 54.
    Soler JJ, Martín-Vivaldi M, Peralta-Sánchez JM, Ruiz-Rodríguez M (2010) Antibiotic-producing bacteria as a possible defence of birds against pathogenic microorganisms. Open Ornithol J 3:93–100CrossRefGoogle Scholar
  55. 55.
    Soler JJ, Peralta-Sánchez JM, Martín-Platero AM et al (2012) The evolution of size of the uropygial gland: mutualistic feather mites and uropygial secretion reduce bacterial loads of eggshells and hatching failures of European birds. J Evol Biol 25:1779–1791. doi: 10.1111/j.1420-9101.2012.02561.x CrossRefPubMedGoogle Scholar
  56. 56.
    Møller AP, Erritzøe J, Tøttrup Nielsen J (2010) Predators and microorganisms of prey: goshawks prefer prey with small uropygial glands. Funct Ecol 24:608–613. doi: 10.1111/j.1365-2435.2009.01671.x CrossRefGoogle Scholar
  57. 57.
    Giraudeau M, Czirják GÁ, Duval C et al (2014) An experimental test in Mallards (Anas platyrhynchos) of the effect of incubation and maternal preen oil on eggshell microbial load. J Ornithol 155:671–677. doi: 10.1007/s10336-014-1050-z CrossRefGoogle Scholar
  58. 58.
    Ding T, Schloss PD (2014) Dynamics and associations of microbial community types across the human body. Nature 509:359. doi: 10.1038/nature13178 Google Scholar
  59. 59.
    Guerrero-Ferreira R, Gorman C, Chavez AA et al (2013) Characterization of the bacterial diversity in Indo-West Pacific loliginid and sepiolid squid light organs. Microb Ecol 65:214–226. doi: 10.1007/s00248-012-0099-6 PubMedCentralCrossRefPubMedGoogle Scholar
  60. 60.
    Hulcr J, Latimer AM, Henley JB et al (2012) A jungle in there: bacteria in belly buttons are highly diverse, but predictable. PLoS One 7, e47712. doi: 10.1371/journal.pone.0047712 PubMedCentralCrossRefPubMedGoogle Scholar
  61. 61.
    Roggenbuck M, Bærholm Schnell I, Blom N et al (2014) The microbiome of New World vultures. Nat Commun 5:5498. doi: 10.1038/ncomms6498 CrossRefPubMedGoogle Scholar
  62. 62.
    Soler JJ, Pérez-Contreras T, De Neve L et al (2014) Recognizing odd smells and ejection of brood parasitic eggs. An experimental test in magpies of a novel defensive trait against brood parasitism. J Evol Biol 27:1265–1270. doi: 10.1111/jeb.12377 CrossRefPubMedGoogle Scholar
  63. 63.
    Martín-Vivaldi M, Peña A, Peralta-Sánchez JM et al (2010) Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc R Soc B 277:123–130. doi: 10.1098/rspb.2009.1377 PubMedCentralCrossRefPubMedGoogle Scholar
  64. 64.
    Sparks NHC (1994) Shell accessory materials: structure and function. In: Board RG, Fuller R (eds) Microbiology of the avian egg. Chapman & Hall, London, pp 25–42CrossRefGoogle Scholar
  65. 65.
    Wellman-Labadie O, Picman J, Hincke MT (2008) Antimicrobial activity of the Anseriform outer eggshell and cuticle. Comp Biochem Physiol 149:640–649. doi: 10.1016/j.cbpb.2008.01.001 CrossRefGoogle Scholar
  66. 66.
    Brandl HB, van Dongen WFD, Darolová A et al (2014) Composition of bacterial assemblages in different components of reed warbler nests and a possible role of egg incubation in pathogen regulation. PLoS One 9, e114861. doi: 10.1371/journal.pone.0114861 PubMedCentralCrossRefPubMedGoogle Scholar
  67. 67.
    Lee WY, Kim M, Jablonski PG et al (2014) Effect of incubation on bacterial communities of eggshells in a temperate bird, the Eurasian Magpie (Pica pica). PLoS One 9, e103959. doi: 10.1371/journal.pone.0103959 PubMedCentralCrossRefPubMedGoogle Scholar
  68. 68.
    Shawkey MD, Firestone MK, Brodie EL, Beissinger SR (2009) Avian incubation inhibits growth and diversification of bacterial assemblages on eggs. PLoS One 4, e4522. doi: 10.1371/journal.pone.0004522 PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    Ruiz-Rodríguez M, Martínez-Bueno M, Martín-Vivaldi M et al (2013) Bacteriocins with a broader antimicrobial spectrum prevail in enterococcal symbionts isolated from the hoopoe’s uropygial gland. FEMS Microbiol Ecol 85:495–502. doi: 10.1111/1574-6941.12138 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Ángela Martínez-García
    • 1
  • Juan J. Soler
    • 1
  • Sonia M. Rodríguez-Ruano
    • 2
  • Manuel Martínez-Bueno
    • 2
  • Antonio Manuel Martín-Platero
    • 2
  • Natalia Juárez-García
    • 3
  • Manuel Martín-Vivaldi
    • 4
  1. 1.Estación Experimental de Zonas Áridas (CSIC)AlmeríaSpain
  2. 2.Departamento de MicrobiologíaUniversidad de GranadaGranadaSpain
  3. 3.EstepaSpain
  4. 4.Departamento de ZoologíaUniversidad de GranadaGranadaSpain

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