Abstract
Intraspecific chemical communication may play a significant role in avian behavior. Preen oil secreted by the uropygial gland emits volatile compounds that vary with many aspects of bird biology and may figure prominently in mate choice. Many of these compounds are known end products of bacterial metabolism in other environments. The fermentation hypothesis for chemical recognition suggests that symbiotic bacteria in mammalian scent glands produce volatile odorants that are used as recognition cues by the host animals and that variation in these bacterial communities contributes to variation in the animal scents. We preliminarily evaluated whether this hypothesis could apply to birds by sampling and sequencing bacterial communities associated with the preen gland of adult breeding dark-eyed juncos (Junco hyemalis). The most common operational taxonomic units (OTUs), defined by the V4 region of the 16S rRNA gene, belonged to the phyla Actinobacteria, Firmicutes, and Proteobacteria. Most of the identified bacterial genera contain species that are known odor producers. Most notably, Burkholderia and Pseudomonas species consistently produce 9 of the 17 volatile compounds whose production is either upregulated during the breeding season or differs between the sexes in juncos. Other genera have documented antifungal or antibacterial properties and may provide other valuable services to the birds. We found no effect of host sex on bacterial community composition or structure. Instead, paired males and females clustered together, suggesting that individuals that have frequent contact may develop similar microbial communities quickly. Our study suggests that the fermentation hypothesis for chemical recognition, originally formulated for mammals, may apply to birds as well, opening new pathways for avian-microbial research.
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Agler MT, Wrenn BA, Zinder SH, Angenent LT (2011) Waste to bioproduct conversion with undefined mixed cultures: the carboxylate platform. Trends Biotechnol 29:70–78
Albone ES, Eglinton G, Walker JM, Ware GC (1974) The anal sac secretion of the red fox (Vulpes vulpes); its chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo). Life Sci 14:387–400
Amo L, López-Rull I, Pagán I, Macías Garcia C (2012) Male quality and conspecific scent preferences in the house finch, Carpodacus mexicanus. Anim Behav 84:1483–1489
Anderson M (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Archie EA, Theis KR (2011) Animal behaviour meets microbial ecology. Anim Behav 82:425–436
Balkwill DL, Fredrickson JK, Romine MF (2006) Sphingomonas and related genera. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 605–629
Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058
Bonadonna F, Bretagnolle V (2002) Smelling home: a good solution for burrow-finding in nocturnal petrels? J Exp Biol 205:2519–2523
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6(8):1621–1624
Caro SP, Balthazart J (2010) Pheromones in birds: myth or reality? J Comp Physiol A 196:751–766
Caspers BA, Krause ET (2010) Odour-based natal nest recognition in the zebra finch (Taeniopygia guttata), a colony-breeding songbird. Biol Lett 7:184–186
Claesson MJ, O’Sullivan O, Wang Q, Nikkilä J, Marchesi JR, Smidt H, de Vos WM, Ross RP, O’Toole PW (2009) Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS One 4(8):e6669
Ezaki T, Li N, Kawamura Y (2006) The anaerobic gram-positive cocci. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 795–808
Ezenwa VO, Williams AE (2014) Microbes and animal olfactory communication: where do we go from here? Bioessays 36:847–854
Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964
Filipiak W, Sponring A, Baur MM, Filipiak A, Ager C, Wiesnhofer H, Nagl M, Troppmair J, Amann A (2012) Molecular analysis of volatile metabolites released specifically by Staphylococcus aureus and Pseudomonas aeruginosa. BMC Microbiol 12:113
Gerlach NM, McGlothlin JW, Parker PG, Ketterson ED (2012) Promiscuous mating produces offspring with higher lifetime fitness. Proc R Soc B 279:860–866
Giraudeau M, Duval C, Guillon N, Bretagnolle V, Gutierrez C, Heeb P (2010) Effects of access to preen gland secretions on mallard plumage. Naturwissenschaften 97:577–581
Gorman ML, Nedwell DB, Smith RM (1974) An analysis of the contents of the anal and scent pockets of Herpestes auropunctatus (Carnivora: Viverridae). J Zool 172:389–399
Green PN (2006) Methylobacterium. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 257–265
Groenhagen U, Baumgartner R, Bailly A, Gardiner A, Eberl L, Schultz S, Weisskopf L (2013) Production of bioactive volatiles by different Burkholderia ambifaria strains. J Chem Ecol 39:892–906
Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319
Hagelin JC, Jones IL, Rasmussen LEL (2003) A tangerine-scented social odour in a monogamous seabird. Proc R Soc B 270:1323–1329
Hammer O (2011) PAST: PAleontological STatistics manual, 2.07 edn. Natural History Museum, Oslo, Norway
Hammer O, Harper DAT, Ryan PD (2001) PAST: PAleontological STatistics software package for education and data analysis. Palaeontol Electron 4:1–9
Jacob JP, Ziswiler V (1982) The uropygial gland. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol 6. Academic, New York, pp 199–324
Jones D, Keddie RM (2006) The genus Arthrobacter. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 945–960
Ketterson ED, Parker PG, Raouf SA, Nolan V Jr, Ziegenfus C, Chandler CR (1997) The relative impact of extra-pair fertilizations on variation in male and female reproductive success in dark-eyed juncos (Junco hyemalis). Ornithol Monogr 1997:81–101
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120
Kulkarni S, Heeb P (2007) Social and sexual behaviours aid transmission of bacteria in birds. Behav Proc 74:88–92
Latorre-Moratalla ML, Bosche-Fusté J, Bover-Cid S, Aymerich T, Vidal-Carou MC (2011) Contribution of enterococci to the volatile profile of slightly-fermented sausages. LWT Food Sci Technol 44:145–152
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
Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM, Scott NM, Gibbons SM, Larsen P, Shogan BD, Weiss S, Metcalf JL, Urselll LK, Vázquez-Baeza Y, Van Treuren W, Hasan NA, Gibson MK, Colwell R, Dantas G, Knight R, Gilbert JA (2014) Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345:1048–1052
Leclaire S, Merkling T, Raynaud C, Mulard H, Bessière J-M, Lhuillier É, Hatch SA, Danchin É (2012) Semiochemical compounds of preen secretion reflect genetic make-up in a seabird species. Proc R Soc B 279:1185–1193
Leclaire S, Nielsen JF, Drea CM (2014) Bacterial communities in meerkat anal scent secretions vary with host sex, age, and group membership. Behav Ecol 25:996–1004
Lemfack MC, Nickel J, Dunkel M, Preissner R, Piechulla B (2014) mVOC: a database of microbial volatiles. Nucleic Acids Res 42(1):D744–D748
López del Castillo-Lozano M, Mansour S, Tåche R, Bonnarme P, Landaud S (2008) The effect of cysteine on production of volatile sulphur compounds by cheese-ripening bacteria. Int J Food Microbiol 122:321–327
Madigan MT, Martinko JM, Stahl DA, Clark DP (2010) Brock biology of microorganisms, 13th edn. Benjamin Cummings, San Francisco
Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144–156
Mardon J, Saunders SM, Anderson MJ, Couchoux C, Bonadonna F (2010) Species, gender, and identity: cracking petrels’ sociochemical code. Chem Senses 35:309–321
Martín-Vivaldi M, Ruiz-Rodríguez M, Soler JJ, Peralta-Sánchez JM, Méndez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M (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
Martín-Vivaldi M, Peña A, Peralta-Sánchez JM, Sánchez L, Ananou S, Ruiz-Rodríguez M, Soler JJ (2010) Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc R Soc B 277:123–130
Moyer BR, Rock AN, Clayton DH (2003) Experimental test of the importance of preen oil in rock doves (Columba livia). Auk 120:490–496
Nolan V Jr, Ketterson ED, Cristol DA, Rogers CM, Clotfelter ED, Titus R, Schoech SJ, Snajdr E (2002) Dark-eyed junco (Junco hyemalis), vol 716, The birds of North America. The Birds of North America, Inc., Philadelphia, PA
Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160
Roze U, Leung KT, Nix E, Burton G, Chapman DM (2010) Microanatomy and bacterial flora of the perineal glands of the North American porcupine. Can J Zool 88:59–68
Saag P, Tilgar V, Mänd R, Kilgas P, Mägi M (2011) Plumage bacterial assemblages in a breeding wild passerine: relationships with ecological factors and body condition. Microbiol Ecol 61:740–749
Saranathan V, Burtt EH (2007) Sunlight on feathers inhibits feather-degrading bacteria. Wilson J Ornithol 119:239–245
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Shaw CL, Rutter JE, Austin AL, Garvin MC, Whelan RJ (2011) Volatile and semivolatile compounds in gray catbird uropygial secretions vary with age and between breeding and wintering grounds. J Chem Ecol 37:329–339
Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349
Shawkey MD, Mills KL, Dale C, Hill GE (2005) Microbial diversity of wild bird feathers revealed through culture-based and culture-independent techniques. Microbiol Ecol 50:40–47
Shawkey MD, Hussain J, Hagelin JC, Vollmer AC, Hill GE (2006) Use of culture-independent methods to compare bacterial assemblages on feathers of crested and least auklets (Aethia cristatella and Aethia pusilla) with those of passerines. Waterbirds 29:507–510
Sheneman L, Evans J, Foster JA (2006) Clearcut: a fast implementation of relaxed neighbor joining. Bioinformatics 22:2823–2824
Sin YW, Buesching CD, Burke T, MacDonald DW (2012) Molecular characterization of the microbial communities in the subcaudal gland secretion of the European badger (Meles meles). FEMS Microbiol Ecol 81:648–659
Soini HA, Schrock SE, Bruce KE, Wiesler D, Ketterson ED, Novotny MV (2007) Seasonal variation in volatile compound profiles of preen gland secretions of the dark-eyed junco (Junco hyemalis). J Chem Ecol 33:183–198
Soini HA, Whittaker DJ, Wiesler D, Ketterson ED, Novotny M (2013) Chemosignaling diversity in songbirds: chromatographic profiling of preen oil volatiles in different species. J Chromatogr A 1317:186–192
Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M, Peralta-Sánchez JM, Méndez M (2008) Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22:864–871
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 3:93–100
Song SJ, Lauber CL, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC, Nakielny S, Gordon JI, Fierer N, Knight R (2013) Cohabiting family members share microbiota with one another and with their dogs. eLife 2:e00458
Spraker JE, Jewell K, Roze LV, Scherf J, Ndagano D, Beaudry R, Linz JE, Allen C, Keller NP (2014) A volatile relationship: profiling an inter-kingdom dialogue between two plant pathogens, Ralstonia solanacearum and Aspergillus flavus. J Chem Ecol 40:502–513
Theis KR, Schmidt TM, Holekamp KE (2012) Evidence for a bacterial mechanism for group-specific social odors among hyenas. Sci Rep 2:615
Theis KR, Venkataraman A, Dycus JA, Koonter KD, Schmitt-Matzen EN, Wagner AP, Schmidt TM, Holekamp KE (2013) Symbiotic bacteria appear to mediate hyena social odors. Proc Natl Acad Sci U S A 110:19832–19837
Towner K (2006) The genus Acinetobacter. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 746–758
Voigt C, Caspers B, Speck S (2005) Bats, bacteria, and bat smell: sex-specific diversity of microbes in a sexually selected scent organ. J Mammal 86:745–749
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Whittaker DJ, Reichard DG, Dapper AL, Ketterson ED (2009) Behavioral responses of nesting female dark-eyed juncos Junco hyemalis to hetero- and conspecific passerine preen oils. J Avian Biol 40:579–583
Whittaker DJ, Soini HA, Atwell JW, Hollars C, Novotny MV, Ketterson ED (2010) Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations. Behav Ecol 21:608–614
Whittaker DJ, Richmond KM, Miller AK, Kiley R, Bergeon Burns C, Atwell JW, Ketterson ED (2011a) Intraspecific preen oil odor preferences in dark-eyed juncos (Junco hyemalis). Behav Ecol 22:1256–1263
Whittaker DJ, Soini HA, Gerlach NM, Posto AL, Novotny MV, Ketterson ED (2011b) Role of testosterone in stimulating seasonal changes in a potential avian chemosignal. J Chem Ecol 37:1349–1357
Whittaker DJ, Gerlach NM, Soini HA, Novotny MV (2013) Bird odour predicts reproductive success. Anim Behav 86:697–703
Acknowledgments
This work was supported by the BEACON Center for the Study of Evolution in Action (NSF Cooperative Agreement DBI-0939454). Fieldwork was supported by a Mountain Lake Biological Station Early Career Fellowship to DJW. All work was conducted in compliance with the Bloomington Institutional Animal Care and Use Committee guidelines (BIACUC protocol 09-037) and with permission from the US Department of Fish and Wildlife, the Virginia Department of Game and Inland Fisheries, and the US Forest Service. We thank Mountain Lake Biological Station, University of Virginia, as well as Mountain Lake Hotel and the Dolinger family for allowing research on their grounds. We thank Nicole Gerlach, Abby Kimmitt, Dustin Reichard, Samuel Slowinski, Sarah Wanamaker, and Joseph Welklin for assistance in the field, John Dover and Arvind Venkataraman for assistance with DNA extraction and sequence processing, and Ellen Ketterson for helpful discussion.
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Whittaker, D.J., Theis, K.R. (2016). Bacterial Communities Associated with Junco Preen Glands: Preliminary Ramifications for Chemical Signaling. In: Schulte, B., Goodwin, T., Ferkin, M. (eds) Chemical Signals in Vertebrates 13. Springer, Cham. https://doi.org/10.1007/978-3-319-22026-0_8
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