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

Roschong Boonyarittichaikij (UGent) , Elin Verbrugghe (UGent) , Daan Dekeukeleire, Diederik Strubbe (UGent) , Sarah Van Praet (UGent) , Robbe De Beelde (UGent) , Lieze Rouffaer (UGent) , Frank Pasmans (UGent) , Dries Bonte (UGent) , Kris Verheyen (UGent) , et al.
(2018) PLOS ONE. 13(10).
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Abstract
he 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.
Keywords
REAL-TIME PCR, BACTERIAL COMMUNITIES, BROOD PARASITISM, ESSENTIAL OIL, EGGS, FECES, QUANTIFICATION, CONTAMINATION

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MLA
Boonyarittichaikij, Roschong, et al. “Mitigating the Impact of Microbial Pressure on Great (Parus Major) and Blue (Cyanistes Caeruleus) Tit Hatching Success through Maternal Immune Investment.” PLOS ONE, vol. 13, no. 10, 2018, doi:10.1371/journal.pone.0204022.
APA
Boonyarittichaikij, R., Verbrugghe, E., Dekeukeleire, D., Strubbe, D., Van Praet, S., De Beelde, R., … Martel, A. (2018). Mitigating the impact of microbial pressure on great (Parus major) and blue (Cyanistes caeruleus) tit hatching success through maternal immune investment. PLOS ONE, 13(10). https://doi.org/10.1371/journal.pone.0204022
Chicago author-date
Boonyarittichaikij, Roschong, Elin Verbrugghe, Daan Dekeukeleire, Diederik Strubbe, Sarah Van Praet, Robbe De Beelde, Lieze Rouffaer, et al. 2018. “Mitigating the Impact of Microbial Pressure on Great (Parus Major) and Blue (Cyanistes Caeruleus) Tit Hatching Success through Maternal Immune Investment.” PLOS ONE 13 (10). https://doi.org/10.1371/journal.pone.0204022.
Chicago author-date (all authors)
Boonyarittichaikij, Roschong, Elin Verbrugghe, Daan Dekeukeleire, Diederik Strubbe, Sarah Van Praet, Robbe De Beelde, Lieze Rouffaer, Frank Pasmans, Dries Bonte, Kris Verheyen, Luc Lens, and An Martel. 2018. “Mitigating the Impact of Microbial Pressure on Great (Parus Major) and Blue (Cyanistes Caeruleus) Tit Hatching Success through Maternal Immune Investment.” PLOS ONE 13 (10). doi:10.1371/journal.pone.0204022.
Vancouver
1.
Boonyarittichaikij R, Verbrugghe E, Dekeukeleire D, Strubbe D, Van Praet S, De Beelde R, et al. Mitigating the impact of microbial pressure on great (Parus major) and blue (Cyanistes caeruleus) tit hatching success through maternal immune investment. PLOS ONE. 2018;13(10).
IEEE
[1]
R. Boonyarittichaikij et al., “Mitigating the impact of microbial pressure on great (Parus major) and blue (Cyanistes caeruleus) tit hatching success through maternal immune investment,” PLOS ONE, vol. 13, no. 10, 2018.
@article{8578251,
  abstract     = {{he 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.}},
  articleno    = {{e0204022}},
  author       = {{Boonyarittichaikij, Roschong and Verbrugghe, Elin and Dekeukeleire, Daan and Strubbe, Diederik and Van Praet, Sarah and De Beelde, Robbe and Rouffaer, Lieze and Pasmans, Frank and Bonte, Dries and Verheyen, Kris and Lens, Luc and Martel, An}},
  issn         = {{1932-6203}},
  journal      = {{PLOS ONE}},
  keywords     = {{REAL-TIME PCR,BACTERIAL COMMUNITIES,BROOD PARASITISM,ESSENTIAL OIL,EGGS,FECES,QUANTIFICATION,CONTAMINATION}},
  language     = {{eng}},
  number       = {{10}},
  pages        = {{13}},
  title        = {{Mitigating the impact of microbial pressure on great (Parus major) and blue (Cyanistes caeruleus) tit hatching success through maternal immune investment}},
  url          = {{http://doi.org/10.1371/journal.pone.0204022}},
  volume       = {{13}},
  year         = {{2018}},
}

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