Mitigating the impact of microbial pressure on great (Parus major) and blue (Cyanistes caeruleus) tit hatching success through maternal immune investment

PLoS One. 2018 Oct 4;13(10):e0204022. doi: 10.1371/journal.pone.0204022. eCollection 2018.

Abstract

The hatching success of a bird's egg is one of the key determinants of avian reproductive success, which may be compromised by microbial infections causing embryonic death. During incubation, outer eggshell bacterial communities pose a constant threat of pathogen translocation and embryo infection. One of the parental strategies to mitigate this threat is the incorporation of maternal immune factors into the egg albumen and yolk. It has been suggested that habitat changes like forest fragmentation can affect environmental factors and life-history traits that are linked to egg contamination. This study aims at investigating relationships between microbial pressure, immune investment and hatching success in two abundant forest bird species and analyzing to what extent these are driven by extrinsic (environmental) factors. We here compared (1) the bacterial load and composition on eggshells, (2) the level of immune defenses in eggs, and (3) the reproductive success between great (Parus major) and blue (Cyanistes caeruleus) tits in Belgium and examined if forest fragmentation affects these parameters. Analysis of 70 great tit and 34 blue tit eggshells revealed a similar microbiota composition (Enterobacteriaceae, Lactobacillus spp., Firmicutes and Bacteroidetes), but higher bacterial loads in great tits. Forest fragmentation was not identified as an important explanatory variable. Although a significant negative correlation between hatching success and bacterial load on the eggshells in great tits corroborates microbial pressure to be a driver of embryonic mortality, the overall hatching success was only marginally lower than in blue tits. This may be explained by the significantly higher levels of lysozyme and IgY in the eggs of great tits, protecting the embryo from increased infection pressure. Our results show that immune investment in eggs is suggested to be a species-specific adaptive trait that serves to protect hatchlings from pathogen pressure, which is not directly linked to habitat fragmentation.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacteria / classification*
  • Bacteria / isolation & purification
  • Bacterial Load
  • Bacteroidetes / isolation & purification
  • Egg Shell / immunology
  • Egg Shell / microbiology*
  • Egg Shell / physiology
  • Enterobacteriaceae / isolation & purification
  • Female
  • Firmicutes / isolation & purification
  • Forests
  • Immunoglobulins / metabolism*
  • Lactobacillus / isolation & purification
  • Muramidase / metabolism*
  • Passeriformes / immunology
  • Passeriformes / microbiology
  • Passeriformes / physiology*
  • Reproduction*
  • Species Specificity

Substances

  • IgY
  • Immunoglobulins
  • Muramidase

Grants and funding

Financial support for this research was provided via the UGent GOA project Scaling up Functional Biodiversity Research: from Individuals to Landscapes and Back (TREEWEB). D. S. is currently funded by a Marie Skłodowska-Curie Action (H2020-MSCA-IF-2015, 706318) and acknowledges the Danish National Research Foundation for support to CMEC (grant number DNRF96). E. V. and L. R. are supported by the Research Foundation Flanders (FWO grant 12E6616N and 11L7514N, respectively). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.