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

Roschong Boonyarittichaikij,Dries Bonte,Kris Verheyen,Frank Pasmans,Robbe De Beelde,An Martel,Daan Dekeukeleire,Diederik Strubbe,Lieze Rouffaer,Sarah Van Praet,Elin Verbrugghe,Luc Lens,Arda Yildirim

doi:10.1371/journal.pone.0204022

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.

Highlights

Embryonic development of birds is a process that is threatened by microbial invasion [1]
The bacterial loads of 70 eggs of great tits collected from nest boxes in 42 plots, and of 34 eggs of blue tits collected in nests from 25 plots were determined by qPCR
We provide evidence for a higher infection pressure in great tit eggs than in those of the sympatric, ecologically similar blue tit, while the bacterial load of neither species was associated with variation in fragment area, egg volume, laying date or clutch size

Summary

Introduction

Embryonic development of birds is a process that is threatened by microbial invasion [1]. The composition of the egg creates a natural physical barrier against bacterial penetration [5], and together with antimicrobial substances within the egg yolk and albumen [6], they constitute a first line of defense. Females can influence the phenotype and fitness of their offspring by modifying the egg composition through the transfer of immunoglobulins (e.g. IgY) and antibacterial proteins to their eggs [7,8]. These maternal immune factors protect the embryo against bacteria which have succeeded in penetrating the eggshell, and the hatchling after the resorption of the remaining egg yolk and albumen. Amongst antimicrobial proteins in the egg albumen, lysozyme, ovotransferrin, and avidin are the three most abundant ones [9]

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