Life history correlates of fecal bacterial species richness in a wild population of the blue tit Cyanistes caeruleus

Abstract

Very little is known about the normal gastrointestinal flora of wild birds, or how it might affect or reflect the host's life-history traits. The aim of this study was to survey the species richness of bacteria in the feces of a wild population of blue tits Cyanistes caeruleus and to explore the relationships between bacterial species richness and various life-history traits, such as age, sex, and reproductive success. Using PCR-TGGE, 55 operational taxonomic units (OTUs) were identified in blue tit feces. DNA sequencing revealed that the 16S rRNA gene was amplified from a diverse range of bacteria, including those that shared closest homology with Bacillus licheniformis, Campylobacter lari, Pseudomonas spp., and Salmonella spp. For adults, there was a significant negative relationship between bacterial species richness and the likelihood of being detected alive the following breeding season; bacterial richness was consistent across years but declined through the breeding season; and breeding pairs had significantly more similar bacterial richness than expected by chance alone. Reduced adult survival was correlated with the presence of an OTU most closely resembling C. lari; enhanced adult survival was associated with an OTU most similar to Arthrobacter spp. For nestlings, there was no significant change in bacterial species richness between the first and second week after hatching, and nestlings sharing the same nest had significantly more similar bacterial richness. Collectively, these results provide compelling evidence that bacterial species richness was associated with several aspects of the life history of their hosts.

Keywords: 16S rRNA; PCR-TGGE; bacterial species richness; fecal microbial community analysis; life-history traits; operational taxonomic unit.

Figure 1

Temperature gradient gel electrophoresis (TGGE) image of bacterial assemblages in faecal samples from ten blue tits, showing variation in paired samples from six female (♀1–6) and four male blue tits (♂1–4), from the 2007 and 2008 breeding seasons (A and B respectively). Arrows indicate the relative positions of the bands detected. M denotes lanes containing the marker λHindIIIEcoR1. A schematic of banding patterns is shown to the right of the gel image.

Figure 2

Frequency distribution of bacterial species richness in blue tits, as determined by the bacterial species richness recorded within individual adults (A) and nestlings (B). There was no significant difference in bacterial species richness between adult male and female blue tits (F_1,52 = 0.02, P = 0.888) nor between nestlings aged 7 or 14 days after hatching (F_1,174 = 0.03, P = 0.859).

Figure 3

Bacterial species richness in the faeces of blue tit adults in breeding pairs. The species richness in males and females within pairs was significantly, positively correlated (r = 0.532, df = 25, P < 0.005). The dashed line represents the 1:1 relationship, where partners in each pair would have the same species richness. The solid line represents the linear regression line of best fit. Some dots represent more than one pair.

Figure 4

Relationship between bacterial species richness and both the number of chicks reared (Clutch Size) and the date that the clutch is initiated (1st Egg Date). Lines represent the predicted values from the model for clutches initiated at various points in the season (1st Egg Date: thickest line = April 24th; thinnest line = May 2nd).

Figure 5

Annual survival of adult blue tits in relation to bacterial species richness and year of sampling showing that survival differed across years and declined with increasing bacterial species richness. Data points and lines are the fitted values from the logistic regression model. Solid symbols and line are for birds sampled in 2007, open symbols and dashed line in 2008.