Skip to main content
Log in

Differences in Culturable Microbial Communities in Bird Nestboxes According to Orientation and Influences on Offspring Quality in Great Tits (Parus major)

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Although bird–microbial interactions have become a topic of increasing research, the influence of nest-site characteristics, such as cavity orientation, on nest microbial communities in free-living passerines has not, to our knowledge, been investigated. This is despite the possibility of microbial differences explaining non-random patterns in nest-site selection and offspring quality, such as those exhibited by great tits (Parus major). We swabbed great tit nestboxes that faced either south–southwest (180–269°) or north–northeast (0–89°). Overall, 28 bacterial species and 11 fungal species were isolated, but the culturable microbial community differed substantially between different orientations—indeed nestboxes could be classified to their orientation group with high accuracy using microbial data. Nestboxes facing south–southwest had a significantly higher fungal load (typically double) than those facing north–northeast due to a higher abundance of two species, Epicoccum purpurascens and Cladosporium cladosporioides. There was no relationship between total bacterial load and orientation, although the abundance of one species, Pseudomonas veronii, was significantly lower in south–southwest boxes. The abundance of the allergen E. purpurascens explained almost 20% of the variation in offspring quality, being significantly and inversely related to chick size (high loads associated with small, poor quality, chicks). Our results provide empirical evidence for a correlation between nestbox orientation and culturable microbial load and a further correlation between abundance of one species, E. purpurascens, and offspring quality. Thus, microbial load, which is itself influenced by nest cavity parameters, could be the proximate factor that influences nest-site choice through its effect on offspring quality (and thus, overall fecundity).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1

Similar content being viewed by others

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE T Automat Contr 19:716–723

    Article  Google Scholar 

  2. Baute MA, Deffieux G, Baute R, Neveu A (1978) New antibiotics from the fungus Epicoccum nigrum. I. Fermentation, isolation and antibacterial properties. J Antibiot 31:1099–1101

    Article  PubMed  CAS  Google Scholar 

  3. Berger S, Disko R, Gwinner H (2003) Bacteria in starling nests. J Ornithol 144:317–322

    Google Scholar 

  4. Bisht V, Arora N, Singh BP, Gaur SN, Sridhara S (2004) Purification and characterization of a major cross-reactive allergen from Epicoccum purpurascens. Int Arch Allergy Immunol 133:217–224

    Article  PubMed  CAS  Google Scholar 

  5. Bisht V, Arora N, Singh BP, Pasha S, Gaur SN, Sridhara S (2004) Epi p 1, an allergenic glycoprotein of Epicoccum purpurascens is a serine protease. FEMS Immunol Med Microbiol 42:205–211

    Article  PubMed  CAS  Google Scholar 

  6. Blanco G, Lemus JA, Grange J (2006) Faecal bacteria associated with different diets of wintering red kites: influence of livestock carcass dumps in microflora alteration and pathogen acquisition. J Appl Ecol 43:990–998

    Article  Google Scholar 

  7. Blazevic DJ, Koepcke MH, Matsen JM (1973) Incidence and identification of Pseudomonas fluorescens and Pseudomonas putida in the clinical laboratory. Appl Environ Microbiol 25:107–110

    CAS  Google Scholar 

  8. Brittingham MC, Temple SA, Duncan RM (1998) A survey of the prevalence of selected bacteria in wild birds. J Wildl Dis 24:299–307

    Google Scholar 

  9. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practice information-theoretic approach. Springer, New York

    Google Scholar 

  10. Burtt EH Jr, Ichida JM (1999) Occurrence of feather-degrading bacilli in the plumage of birds. Auk 166:364–372

    Google Scholar 

  11. Burtt EH Jr (1999) Think small. Auk 116:878–881

    Google Scholar 

  12. Cafarchia C, Camarda A, Romito D, Campolo M, Quaglia N, Tullio D, Otranto D (2006) Occurrence of yeasts in cloacae of migratory birds. Mycopathologia 161:229–234

    Article  PubMed  CAS  Google Scholar 

  13. Cook MI, Beissinger SR, Toranzos G, Rodriguez RA, Arendt WJ (2005) Microbial infection affects egg viability and incubation behavior in a tropical passerine. Behav Ecol 16:30–36

    Article  Google Scholar 

  14. de Hoog GS, Guarro J, Gené J, Figueras MJ (2000) Atlas of Clinical Fungi, 2nd edn. Centraalbureau voor Schimmelcultures, The Netherlands

    Google Scholar 

  15. Droual R, Bickford AA, Walker RL, Channing SE, McFadden C (1991) Favus in a backyard flock of game chickens. Avian Dis 35:625–630

    Article  PubMed  CAS  Google Scholar 

  16. Field AP (2000) Discovering statistics using SPSS for Windows: advanced techniques for beginners. Sage Publications Ltd., London

    Google Scholar 

  17. Garnett MC (1981) Body size, its heritability and influence on juvenile survival among great tits, Parus major. Ibis 123:31–41

    Article  Google Scholar 

  18. Glunder G (2002) Influence of diet on the occurrence of some bacteria in the intestinal flora of wild and pet birds. Deut Tierärztl Woch 109:266–270

    CAS  Google Scholar 

  19. Goodenough AE, Hart AG (2011) Microbiology of bird nest boxes. Microbiologist 31:24–28

    Google Scholar 

  20. Goodenough AE, Stallwood B (2009) Intraspecific variation and interspecific differences in the bacterial and fungal assemblages of blue tit (Cyanistes caeruleus) and great tit (Parus major) nests. Microb Ecol 59:221–232

    Article  PubMed  Google Scholar 

  21. Goodenough AE, Maitland DP, Hart AG, Elliot SL (2008) Nestbox orientation: a species-specific influence on occupation and breeding success in woodland passerines. Bird Study 55:222–232

    Article  Google Scholar 

  22. Goodenough AE, Hart AG, Elliot SL (2008) Variation in offspring quality with cavity orientation in the great tit. Ecol Ethol Evol 20:375–389

    Article  Google Scholar 

  23. Gosler AG (2004) Birds in the hand. In: Sutherland WJ, Newton I, Green RE (eds) Bird ecology and conservation. Oxford University Press, Oxford, pp 85–118

    Chapter  Google Scholar 

  24. Gosler AG, Greenwood JJD, Baker JK, Davidson NC (1998) The field determination of body size and condition in passerines: a report to the British Ringing Committee. Bird Study 45:92–103

    Article  Google Scholar 

  25. Gunderson AR, Forsythe MH, Swaddle JP (2009) Evidence that plumage bacteria influence feather coloration and body condition in a passerine. J Avian Biol 40:440–447

    Article  Google Scholar 

  26. Haywood S, Perrins CM (1992) Is clutch size in birds affected by environmental conditions during growth? Proc R Soc Biol Sci 249:195–197

    Article  CAS  Google Scholar 

  27. Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology, 9th edn. Lippincott Williams and Wilkins, London

    Google Scholar 

  28. Hubálek Z (1978) Coincidence of fungal species associated with birds. Ecology 59:438–442

    Article  Google Scholar 

  29. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monograph 54:187–211

    Article  Google Scholar 

  30. Janiga M, Sedlárova A, Rigg R, Novotná M (2006) Patterns of prevalence among bacterial communities of alpine accentors (Prunella collaris) in the Tatra Mountains. J Ornithol 148:135–143

    Article  Google Scholar 

  31. Kellogg JA, Bankert DA, Withers GS, Sweimler W, Kiehn TE, Pfyffer GE (2001) Application of the Sherlock Mycobacteria identification system using high-performance liquid chromatography in a clinical laboratory. J Clin Microbiol 39:964–970

    Article  PubMed  CAS  Google Scholar 

  32. Kunitsky C, Osterhout G, Sasser M (2006) Identification of microorganisms using fatty acid methyl ester (FAME) analysis and the MIDI Sherlock® Microbial Identification System. In: Miller MJ (ed) Encyclopaedia of rapid microbiological methods (volume III). Parental Drug Association, Bethesda, pp 1–17

    Google Scholar 

  33. Larone DH (1995) Medically important fungi: a guide to identification, 3rd edn. ASM, Washington

    Google Scholar 

  34. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  35. Lombardo MP, Thorpe PA, Cichewicz R, Henshaw M, Millard C, Steen C, Zeller TK (1996) Communities of cloacal bacteria in tree swallow families. Condor 98:167–172

    Article  Google Scholar 

  36. Lucas FS, Heeb P (2005) Environmental factors shape cloacal bacterial assemblages in great tit Parus major and blue tit P. caeruleus nestlings. J Avian Biol 36:510–516

    Article  Google Scholar 

  37. Maul JD, Gandhi JP, Farris JL (2005) Community-level physiological profiles of cloacal microbes in songbirds (Order: Passeriformes): variation due to host species, host diet and habitat. Microb Ecol 50:19–28

    Article  PubMed  CAS  Google Scholar 

  38. McGarigal K, Cushman S, Stafford S (2000) Multivariate statistics for wildlife and ecology research. Springer, New York

    Book  Google Scholar 

  39. Mehmke U, Gerlach H, Kosters J, Hausmann S (1992) The aerobic bacterial flora of songbird nests. Deut Tierärztl Woch 99:478–482

    CAS  Google Scholar 

  40. Mennerat A, Mirleau P, Blondel J, Perret P, Lambrechts MM, Heeb P (2009) Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria. Oecologia 161:849–855

    Article  PubMed  Google Scholar 

  41. Mielnichuk N, Lopez SE (2007) Interaction between Epicoccum purpurascens and xylophagous basidiomycetes on wood blocks. Forest Pathol 37:236–242

    Article  Google Scholar 

  42. Mills TK, Lombardo MP, Thorpe PA (1999) Microbial colonization of the cloacae of nestling tree swallows. Auk 116:947–956

    Google Scholar 

  43. Monrós JS, Belda EJ, Barba E (2002) Post-fledging survival of individual great tits: the effect of hatching date and fledging mass. Oikos 99:481–488

    Article  Google Scholar 

  44. Moreno J, Briones V, Merino S, Ballesteros C, Sanz JJ, Tomás G (2003) Beneficial effects of cloacal bacteria on growth and fledging size in nestling pied flycatchers (Ficedula hypoleuca) in Spain. Auk 120:784–790

    Article  Google Scholar 

  45. Naef-Daenzer B, Widmer F, Nuber M (2001) Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J Anim Ecol 70:730–738

    Article  Google Scholar 

  46. Nuttall P (1997) Viruses, bacteria and fungi of birds. In: Clayton D, Moore J (eds) Host-parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 271–302

    Google Scholar 

  47. Osterhout GJ, Shull VH, Dick JD (1991) Identification of clinical isolates of Gram-negative nonfermentative bacteria by an automated cellular fatty acid identification system. J Clin Microbiol 29:1822–1830

    PubMed  CAS  Google Scholar 

  48. Pendergrass SM (1998) Aerobic bacteria by GC-FAME, Method 0801: NIOSH manual of analytical methods, 4th edn. U.S. Government Printing Office, Washington

    Google Scholar 

  49. Peralta-Sanchez JM, Møller AP, Martin-Platero AM, Soler JJ (2010) Number and colour composition of nest lining feathers predict eggshell bacterial community in barn swallow nests: an experimental study. Funct Ecol 24:426–433

    Article  Google Scholar 

  50. Perrins CM, McCleery RH (2001) The effect of fledging mass on the lives of great tits (Parus major). Ardea 89:135–142

    Google Scholar 

  51. Pinowski J, Barkowska M, Kruszewicz AH, Kruszewicz AG (1994) The causes of the mortality of eggs and nestlings of Passer spp. J Biosci 19:441–451

    Article  Google Scholar 

  52. Rendell WB, Robertson RJ (1990) Influence of forest edge on nest-site selection by tree swallows. Wilson Bull 102:634–644

    Google Scholar 

  53. 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. Microb Ecol 61:740–749

    Article  PubMed  Google Scholar 

  54. Saranathan V, Burtt EH Jr (2007) Sunlight on feathers inhibits feather-degrading bacteria. Wilson J Ornithol 119:239–245

    Article  Google Scholar 

  55. Sharma S (1996) Applied multivariate techniques. Wiley, New York

    Google Scholar 

  56. Shaw P (2003) Multivariate statistics for the environmental sciences. Hodder Arnold, London

    Google Scholar 

  57. Shawkey MD, Mills KL, Dale C, Hill GE (2005) Microbial diversity of wild bird feathers revealed through culture-based and culture-independent techniques. Microb Ecol 50:40–47

    Article  PubMed  Google Scholar 

  58. Shawkey MD, Pillai SR, Hill GE, Siefferman LM, Roberts SR (2007) Bacteria as an agent for change in structural plumage color: correlational and experimental evidence. Am Nat 169:S112–S121

    Article  PubMed  Google Scholar 

  59. Singleton DR, Harper RG (1998) Bacteria in old house wren nests. J Field Ornithol 69:71–74

    Google Scholar 

  60. St Germain G, Summerbell R (1995) Identifying filamentous fungi: a clinical laboratory handbook. Star Publishing, Belmont

    Google Scholar 

  61. Stewart R, Rambo TB (2000) Cloacal microbes in house sparrows. Condor 102:679–684

    Article  Google Scholar 

  62. Tabachnick BG, Fidel LS (1996) Using multivariate statistics, 3rd edn. Harper and Row, New York

    Google Scholar 

  63. Tang Y-W, Ellis NM, Hopkins MK, Smith DH, Dodge DE, Persing DH (1998) Comparison of phenotypic and genotypic techniques for identification of unusual aerobic pathogenic Gram-negative Bacilli. J Clin Microbiol 36:3674–3679

    PubMed  CAS  Google Scholar 

  64. Thompson IP, Bailey MJ, Ellis RJ, Purdy KJ (1993) Subgrouping of bacterial populations by cellular fatty acid composition. FEMS Microbiol Lett 102:75–84

    Article  CAS  Google Scholar 

  65. Tortora GJ, Funke BR, Case CL (2007) Microbiology: an introduction, 9th edn. Pearson, London

    Google Scholar 

  66. von Graevenitz A, Osterhout G, Dick J (1991) Grouping of some clinically relevant Gram-positive rods by automated fatty acid analysis: diagnostic implications. Acta Path Micro Im B 99:147–154

    Google Scholar 

  67. von Graevenitz A, Weinstein J (1971) Pathogenic significance of Pseudomonas fluorescens and Pseudomonas putida. Yale J Biol Med 44:265–273

    Google Scholar 

  68. Wobester GA (1981) Diseases of wild waterfowl. Plenum Press, New York

    Google Scholar 

Download references

Acknowledgements

We thank Hannah Stubbs for laboratory support and the Eric Hosking Charitable Trust for a grant to AEG to fund external microbe identification at specialist laboratories. We also thank two anonymous reviewers for their detailed comments on an earlier version of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anne E. Goodenough.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goodenough, A.E., Stallwood, B. Differences in Culturable Microbial Communities in Bird Nestboxes According to Orientation and Influences on Offspring Quality in Great Tits (Parus major). Microb Ecol 63, 986–995 (2012). https://doi.org/10.1007/s00248-011-9992-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-011-9992-7

Keywords

Navigation